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HISTORY
The anatomic and surgical history of the lymphatic system is shown in Table 29-1.
Table 29-1. Anatomic and Surgical History of the Lymphatic System
Hippocrates
(ca. 460-ca.
360 B.C.)
Described axillary lymph nodes and "white blood" in the nodes
Aristotle (384-
322 B.C.)
Described "fibers which take position between blood vessels and nerves and which contain colorless liquid"
Herophilus of
Chalcedon
300
B.C.
Probably knew about the "milk-bearing vessels" of the mesentery
Erasistratus
(310-250 B.C.)
Described lymphatics of small bowel
Marinus (fl. A.D.
50)
Described mesenteric lymph nodes
Galen (A.D.
129-199)
Described mesenteric lymph nodes and lacteal veins
Paul of Aegina
(A.D. 607-690)
Most likely described infected lymph nodes at the lower neck (scrofulae)
Nicola Massa 1532 By dissecting human cadavers, saw renal lymphatic vessels
Gabriello
Falloppio
(1523-1562)
Described mesenteric "vein" containing yellow matter in dissection on human cadavers
Bartholomeus
Eustachius
1563 From dissecting a horse, described thoracic duct ("vena alba thoracica")
Marco Aurelio
Severino
(1580-1656)
Performed radical mastectomy with axillary dissections
Nicolas C laude
Fabrice de
Peirsc (1580-
1637)
Saw chyliferous vesse ls in dissection of a criminal fed a rich meal before execution
Gaspare Aselli 1622 Based on vivisection of well-fed dog and dissection of mammals, described white cords (the lacteals) containing
milky-appearing liquid
Francis Glisson
(1597-1677)
Theory of absorbent function of lymphatics
Johann Vesling 1634 Based on cadaver studies, produced earliest illustrations of human lymphatics; described thoracic duct
Thomas
Bartholin
1643 First to use the word "lymphatics"
George Joliff
(ca. 1618-
1658)
Recognized that lymphatic vesse ls are throughout the body carrying "aqueous humor"
Jean Pecquet 1647 Based on human and animal dissection, and injection studies, described thoracic duct and cisterna chyli
Johannes van
Horne of
Leyden
1651 During autopsy, accidentally discovered the thoracic duct in man without knowing the work of others
Marcello
Malpighi (1628-
Described conglobate glands along course of lymphatics
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John Bernard
Kinmonth
1952 Developed a clinically applicable lymphangiogram
Denis Parsons
Burkitt
1958 Noted that a tumor of the jaw followed unrecognized lymphoma
Peter Carey
Nowell
1960 Noted mitotic activity of mononuclear leukocytes from human peripheral blood 48 to 72 hours after stimulation
with a red kidney bean extract
R.J.V. Pulvertaft 1964 Described characteristics of cells from Burkitt lymphoma tumor. Later identified the morphology of the Burkitt
lymphoma cell with the phytohemagglutinin-transformed lymphocyte.
Michael AntonyEpstein (1921-
?)
Studied microscopic biopsy specimens and grew cells from Burkitt tumor
Yvonne M. Barr
(?-?)
Sayegh et al. 1966 Used term "sentinel node" to mean the node first visualized following injection of dye (lymphangiography)
R.M. Cabanas 1977 Stated sentinel node concept; demonstrated that sentinel node biopsy could precede lymphadenectomy
Alex & Krag 1993 Reported on ability of radioactive tracers to identify sentinel node
Source: History table adapted from Skandalakis JE. I wish I had been there: highlights in the history of lymphatics. Am Surg 61(9):799-808
1995; with pe rmission.
References:
Alex JC, Krag DN. Gamma-probe guided localization of lymph nodes. Surg Oncol 1993;2:137-143.
Cabanas RM. An approach for the treatment of penile carcinoma. Cancer 1977;39:456-466.
DePalma RG. Disorders of the lymphatic system. In: Sabiston DC Jr. (ed). Textbook of Surgery, 14th Ed. Philadelphia: WB Sauders, 1991.
Gans H. On the discovery of the lymphatic circulation. Angiology 13:530-536, 1962.
Kanter MA. The lymphatic system: an historical perspective. Plast Reconstr Surg 79(1):131-139, 1987.
Knight B. Discovering the Human Body. New York: Lippincott & Crowell, 1980.
Leeds SE. Three centuries of history of the lymphatic system. Surg Gynecol Obstet 144:927-934, 1977.
McGrew RE. Encyclopedia of Medical History. New York: McGraw-Hill, 1985.
Mayerson HS. The lymphatic system w ith particular reference to the kidney. Surg Gynecol Obstet 116(3):259-272.
Sayegh E, Brooks J, Sacher E, Busch F. Lymphangiography of the retroperitoneal lymph nodes through the inguinal route. J Urol
1966;95:102-107.
Schmidt JE. Medical Discoveries: Who and When. Springfield IL: CC Thomas, 1959.
Weinberg JA. Identification of regional lymph nodes in the treatment of bronchiogenic carcinoma. J Thorac Surg 1951;22:517-526.
EMBRYOGENESIS
Normal Development
In spite of the important role that the lymphatic system plays in human physiology and disease, much concerning its genesis
remains an enigma. During the 5th week of gestation, two paired and two unpaired endothelial sacs arise as outgrowths from the
venous channels. These sacs form the primordia of the lymphatic system.
The first primordial lymph sacs to appear are the paired jugular sacs in the neck. They are located bilaterally at the junction of the
subclavian and internal jugular (precardinal) veins. Soon thereafter, extensions from these sacs are visible in the upper limbs. Thenext sac to appear is unpaired and located at the mesenteric root in the retroperitoneal space. Later the unpaired cisterna chyli
develops dorsal to the mesenteric sac. The final paired sacs, two posterior (iliac) sacs, appear at the junction of the sciatic and
femoral veins. In short, it may be said that embryologically the lymph system originates and terminates in the venous system.
By the end of the ninth week, these six lymphatic sacs are linked together by multiple endothelial channels to form a complicated
network of lymphatic vessels (Fig. 29-1). During early fetal development mesenchymal cells invade these sacs, converting them
into groups of lymph nodes. True lymph nodes, however, do not appear until the system of vessels is well established.
Fig. 29-1.
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Development of the lymphatic vesse ls. A. Human embryo at nine weeks, showing the primitive lymph sacs and the developing vessels. B.
Ventral view of the formation of the single thoracic duct from the primitive paired lymphatic plexus. (Modified from Arey LB. Developmental
Anatomy. Rev. 7th Ed. Philadelphia: WB Saunders, 1974. A, after Sabin FR. The development of the lymphatic system. In: Keibel F, Mall
FP, eds. Manual of Human Embryology, vol. 2. Philadelphia: JP Lippincott, 1912. Used with permission.)
The earliest nodes appear in the places occupied by the primary sacs and confluences of capillary plexuses. At first, the nodes are
represented by unencapsulated lymphoid tissue located within the meshwork of lymphatic channels. Later, the lymphoid mass
separates into smaller portions allowing the inward growth of blood vessels and the lymphatic network. Each mass, together with
portions of the surrounding network, becomes enclosed by a capsule of connective tissue. Original lymphoid tissue transforms into
the medullary cords and cortical nodules of the node; the enclosed lymphatic capillaries form the peripheral lymph sinus. Cervical
lymph nodes appear around the 9th week. Later, several other groups of lymph nodes are formed in various areas of the body.
The right and left thoracic ducts are channels connecting the right and left jugular lymph sacs with the cisterna chyli. The cisterna
chyli also connects to the lower intercostal trunks, intestinal trunk, and lumbar trunks. The adult thoracic duct forms between
weeks 6 and 8. It develops from the anastomosis of the right and left thoracic ducts at the level of the 4th to 6th thoracic
segments, the distal (caudal) part of the right thoracic duct, and the proximal (cranial) part of the left thoracic duct. The right
thoracic (lymphatic) duct is formed from the proximal part of the right thoracic duct. It must be noted, however, that the
development presented here is speculative. The reader will find more detailed information in Embryology for Surgeons.2
Embryologically, lymphocytes are derived from the primitive stem cells in the mesenchyme of the yolk sac. From a functional
standpoint, there are two types of lymphocytes: T cells and B cells. The progeny of the lymphopoietic stem cells found in the bone
marrow that are destined to become T cells exit the marrow and settle in the thymus where their differentiation is completed.
Ultimately T cells enter the circulation as the long-lived small lymphocytes. B cells originate in marrow, gut-associated lymphatic
tissue, and the spleen. T cells are responsible for cellular immunity; B cells are responsible for the synthesis of antibodies.
Congenital Anomalies
It is not within the scope of this chapter to discuss lymphatic anomalies in detail. Table 29-2 presents an overview of some of the
more common variations.
Table 29-2. Anomalies of the Lymphatic System
Anomaly Prenatal Age
at Onset
First Appearance (or Other
Diagnostic Clues)
Sex Chiefly
Affected
Relative
Frequency
Remarks
Variations in the course of the
thoracic duct
2nd month No pathologic structures Equal Common
Cystic hygroma (cystic
l m han ioma
6th to 9th
weeks?
At birth or in infancy Equal (neck); male
roin
Uncommon Invasive growth; may
be a neo lasm
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Primary lymphedema: Milroy's
disease
3rd month? At birth Equal? Rare Familial tendency
Lymphedema precox 3rd month? At any age Equal? Rare
Mesenteric, omental and
retroperitoneal lymphatic cysts
? In infancy to middle age Male (children);
female (adults)
Uncommon
Source: Skandalakis JE, Gray SW. Embryology for Surgeons, 2nd Ed. Baltimore: Williams & Wilkins, 1994; with permission.
Congenital anomalies of the lymphatic system are relatively rare. One condition is seen as diffuse swelling of some portion(s) of the
body called "congenital lymphedema." Whether this is due to congenital hypoplasia of the lymphatic vessels or from dilatation of the
primitive lymphatic vessels is still to be established. Less commonly, there are cases of diffuse cystic dilations of the lymph vessels
which exist widely throughout the body.
We quote from Musone et al.3:
Cystic hygroma is a malformation of the lymphatic system that is diagnosed by ultrasound very well from the first quarter of
pregnancy. It is frequently associated with chromosomal and non-chromosomal abnormalities. The presence of septae in it
and amniotic fluid alpha-fetoprotein levels are prognostic indicators.
Hygromas (cystic lymphangiomas) develop as large swellings in the lower neck. Hygromas are large cavities filled with fluid which
may appear at birth and frequently grow and make their presence known in the infant. Riquet et al.4 distinguish between tissular
lymphangiomas of the neck and mediastinum found in childhood through young adulthood, and the purely liquid cysts of the
posterior or middle mediastinum of older adults. The former are congenital, the latter suggest an acquired origin. Hygromas,
according to Moore and Persaud,5 apparently are derived from abnormalities in the jugular lymph sacs. Hygromas may be pinched
off parts of the lymph sacs or may be lymphatic spaces which never established connections with lymph channels.
Pulmonary lymphangiectasia, a rare disease characterized by abnormal pulmonary lymphatics, was studied by Bouchard et al.6 They
reported that although it is fatal in the neonatal period, survival is possible and symptomatology decreases with age.
SURGICAL ANATOMY
The various elements of the lymphatic system, such as the ring of Waldeyer (tonsillar ring), thymus gland, spleen, bone marrow,
and lymphatic follicles of the respiratory, genitourinary, and alimentary systems are discussed in other chapters. In addition, the
lymphatic drainage of each organ and region of the trunk is discussed in chapters pertinent to them. The primary purpose of this
chapter is to present anatomic information which is related to surgery, rather than describing the lymphatic system in toto.
The lymphatic system can be divided into two broad categories: the lymphatic network at large and the lymphatic organs.
The lymphatic network at large includes:
The complicated network of irregular capillaries, consisting of minute lymph vesse ls that drain the lymph of the body (with the exception
of hyaline cartilages , epidermis, and the eye's cornea)
Larger lymph vessels which drain the capillaries
Lymph glands which accept lymph from the lymph vessels and filter the lymph
Large lymph vessels which are responsible for draining the lymph into the veins
The lymphatic entities to be studied in this chapter are:
Cisterna chyli
Thoracic duct
Right lymphatic duct
Cisterna Chyli
Is the cisterna chyli a typical and constant anatomic entity? Anatomists disagree. An illustration in Gray's Anatomy 7 designates the
cisterna chyli as "atypical" and "unusual." Woodburne and Burkel,8 quoting Nelson, indicate that the cisterna chyli is present in 25
' 9
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.
demonstrated. Lee McGregor's Synopsis of Surgical Anatomy 10 describes it as being present in 50 percent of cases. The authors o
this chapter will designate as "cisterna chyli" a dilatation of the proximal thoracic duct or perhaps confluence of lymphatic trunks
that may form a sac.
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 receives the right and left lumbar
trunks, the intestinal trunk, and the lowest intercostal vessels (Figs. 29-2 and 29-3).
Fig. 29-2.
The general plan of the lymphatic system. (Modified from Woodburne RT, Burkel WE. Essentials of Human Anatomy (9th ed). New York:
Oxford University Press, 1994; used with permission.)
Fig. 29-3.
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Formation of the cisterna chyli by several trunks and proximal thoracic duct. (Modified from Brantigan OC. Clinical Anatomy. New York:
McGraw-Hill Book Co., 1963; used with permission.)
Multiple sacculations may be present as a result of the contributing vessels. However, sacculations are not present after the
convergence of the contributing 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. To diagnose such a giant c isterna chyli,
MRI with gadolinium-DTPA enhancement has been used.11
The right and left lumbar trunks transmit lymph from the abdominal wall below the level of the navel, pelvis, kidneys, and adrenal
glands. The intestinal trunk, which receives the lymph and chyle from the parts of the gastrointestinal tract supplied by the celiac
and superior mesenteric arteries, occasionally empties directly into the so-called 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.
Thoracic Duct
The thoracic duct is approximately 45 cm long and 2-5 mm in diameter. 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 t runks.
The duct can be subdivided into three parts: abdominal, thoracic, and cervical. The abdominal part of the thoracic duct originates
from the c ranial 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 hemiazygosand accessory hemiazygos veins are posterior to the thoracic duct; the esophagus, diaphragm and pericardium are anterior to it.
At the level of T7 (Fig. 29-4), the thoracic duct travels obliquely behind the esophagus to the level of the f ifth thoracic vertebra.
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 duct passes posterior to the common carotid artery, internal jugular vein, vagus
nerve, left anterior scalene muscle, and left phrenic nerve. It passes anterior to the vertebral artery and vein and the sympathetic
trunk. The duct proceeds upward to the level of C7, whereupon it descends across the subclavian 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. A rare large thoracic duct
cyst that expanded into the anterior cervico-thoracic junction has been reported by Karajiannis et al.12
Fig. 29-4.
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The oblique thoracic course of the definitive thoracic duct, resulting from the anastomosis of the right and left thoracic ducts. Thedefinitive duct represents the retention of the proximal part of the right thoracic duct and the distal segment of the left thoracic duct.
The thoracic duct is the largest lymphatic channel in the body. It collects lymph from the entire body except the right hemithorax
(thoracic wall, right lung, right side of the heart, part of the diaphragmatic surface of the liver, lower area of the right lower lobe of
the liver), right head and neck, and right upper extremity. The volume of flow through the thoracic duct is between 60 and 190
cc/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 two weeks, as collateral channels reroute the flow. 13
Regurgitation of blood from the jugulosubclavian confluence into the thoracic duct is not possible in life because the opening of the
thoracic duct into t he subclavian vein is protect ed 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.
There are several variations in the termination of the thoracic duct (Figs. 29-5 and 29-6). In 1959 Jdanov14 reported termination in
the following sites:
Internal jugular vein 48%
Subclavian vein 9%
At the junction of the internal jugular and subclavian veins 35%
Left brachiocephalic (innominate) vein 8%
Fi . 29-5.
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Variations of the entry of the thoracic duct into the venous system. a. A single thoracic duct and a s imple 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 Heberer G, van Dongen RJAM (eds). Vascular Surgery. Berlin, Heidelberg: Springer-Verlag, 1989; used with permission.)
Fig. 29-6.
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Photographs of the various types of endings of the trunk of the thoracic duct. A. Type A-1. The duct is directly inserted into the venous
angle. B. Type A-2. The duct separates into two trunks before and after running below the left brachiocephalic vein. C. Type A-3. The duct
has two trunks, one extending to the beg inning of the subclavian vein and the other to the venous angle. D. Type B-1. The duct with two
trunks runs directly to the internal jugular vein. E. Type B-2. The duct separates into three trunks after running below the left
brachiocephalic vein; one trunk runs to the internal jugular vein, and the others (two branches) to the subclavian vein. F. Type C-1. One
trunk is inserted into the external jugular vein and the othe r into the subclavian vein. G. Type C-2. One trunk is inserted into the external
jugular vein and the o ther into the internal jugular vein. H. Type D. There are four trunks and they are inserted into the beginning of the
internal and external jugular veins, and into the subclavian vein. ejv, external jugular vein; ijv, internal jugular vein; lbv, left
brachiocephalic vein; sv, subclavian vein. (From Shimada K, Sato I. Morphological and histological analysis of the thoracic duct at the
jugulo-subclavian junction in Japanese cadavers. Clin Anat 1997;10:163-172; used with pe rmission.)
Kinnaert15 dissected 49 cadavers and collected 480 additional cases. He reported the termination of the thoracic duct as follows:
No evidence of left thoracic duct 0-4.5%
Multiple terminal openings:
In others' cases 10-40%
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 Sato16 found that only 38% of Japanese had thoracic ducts that terminate in the jugulosubclavian angle. In
comparison, previous studies by Kihara and Adachi17 found this occurrence in 78.2% of Japanese and in 33% of European subjects
Shimada and Sato noted the following sites and frequencies of termination of the trunk of the thoracic duct (Fig. 29-6), each majo
type also possessing subtypes not discussed here:
Venous angle 38%
Internal jugular vein 27%
External jugular vein 28%
Other, complex configurations 7%
Shimada and Sato16 noted that while the multiple complex configuration occurred only 7% of the time, this termination was highly
correlated 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.
In Clinical Anatomy and Pathology of the Thoracic Duct: An Investigation of 122 Cases,18 Jacobsson presented a very useful
summary of the thoracic duct which we reprint here with gratitude.
An anatomical study was made of the thoracic duct in 100 autopsy cases. A thoracic duct was found in every case and
always started below the diaphragm, passed the posterior mediastinum in the thorax and discharged into the confluence of
the veins in the left of the neck. In 4% of the cases a branch left the thoracic part of the thoracic duct at the aortic arch
and emptied into the veins in the right side of the neck.
The beginning of the thoracic duct conformed to one of four types, depending on how the lumbar and intestinal trunks
combined into the abdominal part. In 20% the thoracic duct arose from the confluence of the lumbar and intestinal trunks
and in 55% it was formed after the intestinal trunk, branched or un-branched, had joined either the thoracic duct or one or
both lumbar trunks. In 24% the thoracic duct ascended from a plexus formed by the lumbar and intestinal trunks. In 1% the
thoracic duct had a plexiform structure throughout its course.
A cisterna chyli was found in 52% of the cases, with a roughly uniform distribution by sex. Its diameter averaged 6.7 mm but
varied between 4 and 14 mm. In the thoracic part, insulae and plexus formations of the thoracic duct were found in 32%.
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The cervical part of the thoracic duct corresponded to one of 9 types, A, B and C having a single trunk with one (36%), two
(13%) and three (3%) openings respectively into the venous system, D, E and F one or several insulae and one (18%), two
(3%) and three (1%) openings respectively into the venous system, and G, H and I one or several plexuses and one (14%),
two (9%) and three (3%) openings respectively, into the venous system on the left side of the neck. A total of 139
openings into the left veins in the neck were found in the l00 specimens of the thoracic duct. The most common site was
the left subclavian vein (64), followed by the left venous angle (51), the left internal jugular vein (22) and the left external
jugular vein (2).
Small lymph vessels emptied into the thoracic duct along its entire length and close connections were found with lymph
nodes. Left jugular and subclavian trunks were often detected in the cervical part, emptying into the thoracic duct or
independently into the cervical veins.
The thoracic duct was found to be irregular and its diameter was not constant, usually being greatest in the cervical part
(excluding the cisterna chyli) and smallest in the lower thoracic part. Measurements at five levels gave the following average
cross-sectional areas: (1) 14.7 sq. mm one centimeter from the opening into the venous system, (2) 11.5 sq. mm one-third
of the way from the termination to the aortic arch, (3) 6.4 sq. mm at the aortic arch, (4) 4.5 sq. mm midway between the
aortic arch and the diaphragm, and (5) 7.0 sq. mm one centimeter below the diaphragm. The largest and smallest external
diameters measured in the cervical part were 8 mm and 1.5 mm.
Constrictions were observed along the thoracic duct, usually corresponding to the location of bi-cuspid valves in the vessel.
The valves became more numerous as one approached the opening into the venous system, averaging 4.6 below the
diaphragm, 5.9 between the diaphragm and the aortic arch, and 11.1 between the aortic arch and the termination of the
thoracic duct. A terminal valve at the opening into the left cervical veins was found in 82 instances, no valve at all in the
vicinity of this junction in 2 instances and a valve 1-6 mm from the opening in 55 instances.
Right Lymphatic Duct
The right lymphatic duct "typically" begins with the union of three lymphatic trunks: right jugular, right subclavian, and right
bronchomediastinal (Figs. 29-7 and 29-8).
Fig. 29-7.
Variations of the lymphatic junctions a t the right venous angle. A. Entry of the tributaries into the right lymphatic duct. B. Partial entry
into the right lymphatic duct. C. Separate entry of the tributaries near the right venous angle. (From Heberer G, van Dongen RJAM (eds).
Vascular Surgery. Berlin, Heidelberg: Springer-Verlag, 1989; used with permission.)
Fig. 29-8.
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Variations in the terminal lymph trunks of the right side. a = jugular trunk; b = subclavian trunk; c = bronchomediastinal trunk; d = right
lymphatic duct; e = lymph node of parasternal chain; f = lymph node of deep cervical chain. (Modified from Williams PL (ed). Gray's
Anatomy (38th ed). After Po irier & Charpy. New York: Churchill Livingstone, 1995; used w ith permission.)
The right bronchomediastinal trunk is regarded as the vestigial portion of the terminal (cranial) segment of the embryologic right
thoracic duct. It receives lymphatic drainage from the right lung, lower left lung, right diaphragm, 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 related to the anterior scalene muscle. In the majority of
cases, the right lymphatic duct empties into the junction of the right subclavian and right internal jugular veins. However, as
demonstrated in Figures 29-7 and 29-8, its termination also has numerous variations.
HISTOLOGY AND PHYSIOLOGY
Lymph capillaries are very thin. They unite to form lymphatic vessels. Lymph capillaries are lined by endothelium and are slightly
larger than blood capillaries. They are unique, however, in that they lack a continuous basal lamina and are permeable only in one
direction. The edges of adjacent endothelial cells overlap significantly, providing an intercellular cleft with one or two tiny points of
closer apposition and adherence.
Extracellular bundles of filaments extend outward from the endothelium between collagen bundles of the surrounding connective
tissues. These bundles are believed to play a role in keeping the lumen of the vessel open. Furthermore, it is presumed that as
interstitial fluid increases around the lymphatic capillary, the "anchoring" filaments open the clefts, allowing the inward flow of
intercellular fluid and even large molecules. As a result, relatively large products of metabolism can enter the lymph vessel,
thereafter being pushed by the contraction of surrounding muscles and interstitial pressures.
The pathway of lymph starts in interstitial tissue spaces where lymph accumulates, perhaps secondary to the slight predominance
of capillary filtration and reabsorption. Lymph passes from lymph capillaries to lymphatic vessels by propulsion and contraction. The
lymphatic vessels carry the fluid to the lymph nodes by way of the nodal sinuses. Efferent vessels carry the lymph to the next
node in the chain, and eventually the fluid flows to lymph trunks. The trunks pass the lymph into the thoracic and right lymphatic
duct, where it reaches the venous circulation.
If some lymph vessels are damaged or blocked, new vessels form readily. The system drains broadly into the venous system. It is
well understood that the t horacic duct and the right lymphatic duct open into their respect ive brachiocephalic veins, but those
who have studied these vessels report openings of lymph vessels into the inferior vena cava, renal, suprarenal, azygos, and iliac
veins.
Lymph capillaries and lymphatic vessels have one-way valves which open upon contraction of the vascular wall. These valves
permit the passage and circulation of lymph fluid (3 to 5 liters daily) into larger vessels and, ultimately, to the thoracic ducts. The
valves are bicuspid and prevent backflow.
Lymphatic vessels always follow minute arteries and veins. They resemble veins in structure but have thinner walls, more valves,
and contain lymph nodes at various intervals along their length.
The exact number of lymph nodes in the body is not known and estimates vary greatly. According to Gray's Anatomy,7 a normal
young adult body contains some 400-450 lymph nodes, distributed approximately as follows: head and neck, 60-70; thorax, 100;
abdomen and pelvis, 230; arm and thoracoabdominal wall (supraumbilical area), 30; leg and lower abdominal wall and superficial
buttocks and perineum, 20. Conversely, Bailey and Love's Short Practice of Surgery 19 reported a total of 800 lymph nodes, 300 of
which are located in the neck.
Lymph nodes are responsible for filtering lymph and producing antibodies by responding to antigens. Nodes vary greatly in size,
ranging from 1-2 mm to 3-4 cm in diameter.20 Each node (Fig. 29-9) is covered by a capsule of dense connect ive tissue which
sends trabecular extensions to the center of the lymph node. The nodal parenchyma is divided into two regions: cortex and
medulla.
Fig. 29-9.
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A semi-schematic frontal section of a lymph node. (Modified from Woodburne RT, Burkel WE. Essentials of Human Anatomy, 9th Ed. New
York: Oxford University Press, 1994; with permission.)
The cortex is the outer and more densely staining part of the lymph node. The cortex contains lymph nodules or follicles
(aggregations of lymphocytes) which contain lighter staining germinal centers. According to Roth and Reith,21 the germinal center
is a "morphological indication of lymphatic tissue response which ultimately leads to lymphocyte, plasma cell, and antibody
formation." The germinal center may be the site of genesis of the immune system.
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e nnermos par o e ymp no e s e me u a. e ymp o ssue o e me u a s organze n o me u ary cor s an
medullary sinuses. The medullary cords consist of reticular fibers and cells that develop around tiny blood vessels. Accordingly,
small lymphocytes, macrophages, and mature plasma cells can be found in association with medullary c ords. The medullary sinuses
converge in the vicinity of efferent lymphatic vessels and serve to drain the lymph node. Stellate cells found within the sinuses
form a weblike series of microscopic baffles, allowing interaction with macrophages in the wall of the sinus. This interaction may
create a trap for cells passing through the lumen of the sinus.
The lymphatic and blood vascular systems are fellow travelers, with multiple interactions in health and disease. There are two
principal pathways by which malignant cells spread via the lymphatic system:
Permeation of minute lymphatic vessels, which ultimately leads to growth and spread to regional lymph nodes
Lymphatic metas tasis by tumor cell emboli, which may bypass a lymph node or become entrapped in the lymph node
The lymph nodes may act as temporary filters, in which metastatic malignant cells are trapped, propelled into vessels, or
destroyed.
It is known that lymph nodes can effectively arrest the passage of particulate matter and blood cells, and entrap and destroy
bacteria. Some viruses, however, can proliferate rapidly within the lymph node and thereafter easily disseminate throughout the
body. Similarly, lymph nodes may fail to entrap other kinds of cells carried in the lymph. For example, a large percentage of cancer
cells may transit in lymphatic vessels without being arrested at the node.
When malignant cells are entrapped within the node they may proliferate rapidly, greatly increasing the size of the node. Non-
tender, hard, compacted masses of nodes usually contain metastatic carcinoma or very aggressive intrinsic neoplasms. The
particular location of the lymph gland enlargement often provides very definite clues as to the location and nature of the primary
lesion.
Read an Editorial Comment
Remember
Interstitial fluid from the brain and spinal cord, especially the gray matter, drains through perivascular spaces and paravascular
compartments of the subarachnoid space to reach the regional lymph nodes. For example, cervical lymph nodes receive interstitial fluid
drainage from the brain, while lumbar lymph nodes receive interstitial fluid drainage from the spinal cord.
Lymphatic capillaries are present along the peripheral nerves. Lymphatics are scanty, but present, in the periosteum of bone and in
tendons.
Many anomalies and variations occur within the origin, distribution, and termination of the thoracic duct.
When the thoracic duct itself enters the venous system on the right, there is frequently an anomalous retroesophageal right subclavian
artery.
All the lymphoid tissue of the human body forms approximately 1% of the body we ight (about ó the weight of the liver).
The cisterna chyli and the right lymphatic duct and thoracic duct can be ligated with impunity.
Lymphocytes and lymph always circulate w ithin the nodal parenchyma.
On its pathway to the neck, the thoracic duct is not interrupted by lymph nodes; therefore, lymph which is a lready filtered by several
groups of lymph nodes is drained directly into the veins.
Since the valves do not work after death, blood can regurgitate into the ducts, causing the involved segments to resemble veins.
After injury or ligation of a lymphatic vessel, the lumen of the vessel becomes solid, and later the endothelium recanalizes.
Acquired cutaneous lymphangiectasia, w ith areas o f skin affected by obstruction and destruction of lymphatic drainage, was reported by
Garcia-Doval et al.,22 who stated that this was the first case associated w ith altered lymph flow in cirrhosis and ascites.
We quote from Gidvani et a l.,23 who stressed the need to include Castleman's disease in the differential diagnosis of pediatric
lymphoproliferative disorders:
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Cast emans sease a so nown as ang o o cu ar ymp no e yperp asa, ang omatous ymp o amartoma, an g ant
lymph node hyperplasia) is an uncommon lymphoproliferative disorder that most frequently is seen as an asymptomatic mass
in the mediastinum. Little is known about the cause of this disorder, but the bulk of the evidence points toward faulty
immunoregulation, which results in the excessive proliferation of B lymphocytes and plasma cells in lymphoid organs.
Rarely, the cisterna chyli may suffer isolated injury in blunt abdominal trauma.24
SURGERY
In this book, surgery of the lymphatic system (lymphadenectomy) is presented in the chapters of the concerned organs.
Though it is not within the scope of this chapter to cover lymphedema, the senior author of this chapter (JES) asks the reader's
indulgence to reminisce about 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.
ANATOMIC COMPLICATIONS
Iatrogenic injury during surgery, or penetrating injuries of the neck, thorax, and upper abdomen may injure the thoracic duct and
lead to chylorrhea. The thoracic duct may be injured at its beginning, middle, or terminal portion during a number of surgical
procedures, including but not limited to:
Hiatal hernia repair
Distal esophageal surgery
Surgery of aortic aneurysm
Esophageal resection
Thoracic aortic aneurysm surgery
Scalene biopsy
Left radical neck surgery
Acc ording to Woodburne and Burkel,8 injuries to the thoracic duct can produce 75-200 cc of chylous drainage per hour. This is
enough fluid to soak the patient's pillow and upper bed if it drains out, to collapse the lung (chylothorax), or to produce an
enlarged abdomen (chyloperitoneum).
Chylous draining may oc cur during neck surgery or with penetrating injuries. It may be persistent or temporary. If the draining is
persistent, ligation is essential.
Nussenbaum and colleagues25 performed a patient trial of conservative treatment of chyle fistula, including nutritional modification,
pressure dressings, and closed drainage. This medical management failed in 20%. They support early operative intervention if the
peak 24-hour drainage is greater than 1000 mL: "Persistent low-output drainage after 10 days is associated with a prolonged
management course and treatment-related complications. Optimal treatment of these patients is unclear."
We quote from Gregor26 on the management of chyle fistula:
Total parenteral nutrition allows for control of the fluid and protein loss while avoiding flow of chyle, and in most cases it
results in resolution. In those cases that do not resolve, fibrin glue with some type of mesh and muscle flaps usually succeed
in closure.
If the thoracic duct is injured within the thorax, chylothorax with secondary collapse of the left lung can result. If repeated
aspiration is unsuccessful, ligation is needed not only to avoid restriction of the lung but also to avoid chylous ascites and
decreased nutrition.
Thoracoscopic ligation of the thoracic duct has been used to treat chylothorax following esophagectomy.27 For the same
condition, Merigliano et al.28 advocate early thoracic duct ligation, with re-operation performed immediately after diagnosis. Sakata
et al.29 treated primary chylopericardium by thoracoscopic thoracic duct ligation and partial pericardiectomy.
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Chylous ascites can occur secondary to injury of the cisterna chyli or the proximal subdiaphragmatic part of the thoracic duct.
With chylous ascites, the abdominal cavity becomes tremendously enlarged due to accumulation of fluid. Again, ligation is
necessary.
Beghetti et al.30 studied the etiology and management of pediatric chylothorax:
Prevention, early recognition, and treatment of potential complications, such as superior vena cava thrombosis or
obstruction, may further improve success of conservative treatment. Congenital chylothorax seems different and may require
a specific approach.
It is well known that radiation treatment, as well as some surgical procedures, produces dilatation of the lymphatic vessels, the so-called acquired lymphangiectasis. Celis et al.31 treat this complication with CO2 laser ablation with good results.
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