5. ANATOMY OF THE HUMAN LYMPHATIC SYSTEM

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5. ANATOMY OF THE HUMAN LYMPHATIC SYSTEM

MAURO ANDRADE AND ALFREDO JACOMO Department of Surgery, University of Sao Paulo, Brazil

INTRODUCTION

The lymphatic system transports lymph from interstitial space in different organs toward the base of the neck. Its pathway begins after resorption from initial lymphatics and lymph transport to progressively larger vessels (lymphatic collectors and trunks), finally reaching the confluence of the internal jugular and subclavian veins as lymphatic and thoracic ducts, respectively, at the right and left venous angles.

Even though important physiopathological and therapeutical issues may exist due to the close anatomical, embryological, and functional relationship of blood and lymphatic vessels, there are some marked differences between the two systems (1).

In that sense, unlike blood vessels, the lymphatic system cannot be considered as a real circulatory system. While blood circulates in a closed circle pumped by the heart, both in systemic and pulmonary circulation, lymph flow is unidirectional from peripheral tissues to blood and is considered to be an open semicircular system.

The lymphatic system is ubiquitous and exists in all tissues where blood vessels are also found, placenta being an exception. Cornea does not contain lymphatics (10).

For a long time, the existence of lymphatics in the central nervous system has been a subject of discussion among anatomists. However, liquor is now considered as the neuroaxis lymph and it has a clear relationship with cervical lymphatic pathways.

Study of lymphatics has always been troublesome for the anatomists due to the small caliber of the lymphatic vessels and their transparent content. After the initial observation of the chylous vessels by Aselli in 1627, methods were developed to observe the lymph vessels. In the seventeenth century, mercurial injections were

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56 Cancer Metastasis and the Lymphovascular System

employed and Gerota’s solution, idealized at the end of the nineteenth century, is still in use today with some modifications (3, 6–9).

GENERAL ORGANIZATION OF THE LYMPHATIC SYSTEM

The fluid originated from capillary filtration flows preferentially through the tissue channels, the “microcirculatory highway” of the interstitium. After absorption of the interstitial fluid by the initial lymphatics, lymph is transported through progressively larger and structurally more complex vessels until its final destination into the blood system.All along the way, compact chains of capsulated lymphocytes, the lymph nodes, filter the lymph and are responsible for another essential role of the system: the immune response (14).

According to Kubik, lymphatic vessels can be classified in a crescent order of size and complexity in lymph capillaries, precollectors, collectors, and trunks. The first two are denominated initial lymphatics (12).

The structure of lymph capillaries, whose prime function is absorption of fluid and macromolecules, differs from blood capillaries in some essential features: their format resembles glove fingers, they have incomplete basal membrane, and are larger than the correspondent blood capillary vessels (1).Their endothelial cells have a small number of open junctions, not found in blood vessels (except for sinusoidal capillaries and injured vessels). In some areas, adjacent endothelial cells partially overlap, creating a point of entry for interstitial fluid and at the same time acting as an antireflux mech- anism. Anchoring filaments are a unique anatomical feature presented by lymph capillaries; these structures are extensions of the endothelial cells and originate on the outer surface of the intercellular contact area between two adjacent cells. Their adhesions to interstitial elastic and collagen fibers open the intercellular space when interstitial volume increases and are a major feature of lymph absorption.

Collector vessels and trunks present structure similar to veins, even though their three layers – intimae, media, and adventitia – are thinner and have a less evident separation than those observed in the venous system. They have semilunar valves, more numerous and histologically similar to the vein valves, formed by folds of endothelium, smooth muscle, and connective tissue.There is also a valve at the lymphatic confluence at the jugulosubclavian junction, thus avoiding blood reflux to the major lymphatic ducts (10 ).

The lymphatic system, according to its topography, can be divided into three systems:

superficial, deep, and visceral.The superficial system drains skin and subcutaneous tissue whereas the deep lymphatic system is responsible for the subfascial tissue drainage.The visceral system can also be considered a part of the deep system. Perforating vessels cross the fascia and connect the superficial and deep systems. Some authors consider another group of vessels: the communicating vessels, which communicate areas drained by different bundles. Lymphatic collectors of the limbs, both superficial and deep, accompany neighboring vessels (2), the drained volume through the superficial system being far more important to the lymphatic drainage of the extremities.

Lymph nodes consist in an agglomerate of lymphoid tissue surrounded by a capsule of dense connective tissue and some smooth muscle fibers and their inner framework is

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5. Anatomy of the Human Lymphatic System 57

formed by trabeculae, extensions of the inner aspect of the capsule that limit lymph follicles.After reaching the lymph node, lymph flows through its subcapsular space and is filtered in the network formed by the trabecular and medullar sinuses. Lymph nodes are arranged as chains found in reasonably constant areas of the body and contain a variable number of nodes; the total number of lymph nodes in humans is estimated to be around 600–700 (13).The shape of the lymph nodes is usually spherical or round, and can vary considerably in size, and may reach a normal diameter of up to 1 in. Structurally, they have a small depression called the hilus and an opposite convex surface. Efferent lymph vessels and nodal arteries and veins are found in the hilus whereas afferent lymph vessels reach the lymph node in many points along its convex surface.Afferent lymph vessels are generally smaller and more numerous than the efferent vessels (14).

The same as in lymph vessels, lymph node groups, or chains can be classified according to their location as superficial, when they are embedded into the subcutaneous tissue, or deep, situated under the muscular fascia or inside abdominal or thoracic cavities (2).

FORMATION OF THE MAIN LYMPHATIC TRUNKS AND DUCTS

There are 11 lymphatic trunks: gastrointestinal, lumbar, bronchomediastinal, subclavian, jugular, and descending intercostals (10). All, except for the gastrointestinal trunk, are paired.

Lumbar trunks are formed by the union of lymphatic vessels, which drain the following regions: lower limbs, urogenital system, anatomical structures irrigated by the inferior mesenteric artery, and the infraumbilical portion of the abdominal wall.

Efferent lymph vessels from celiac and superior mesenteric lymph nodes originate the gastrointestinal trunk.

The right and left bronchomediastinal trunks are responsible for the transport of lymph coming from the deep layer of the superior and anterior areas of the abdomen and thorax, the anterior portion of the diaphragm, lungs, heart, and visceral aspect of the right lobe of the liver.

The subclavian trunks are formed by lymphatic collectors draining the upper limbs, supraumbilical area of the abdominal wall, and anterior thoracic wall.

Lymph from the head, face, inner structures of the neck, and posterior cervical region drain toward the jugular trunks.

The descending intercostal trunks collect the lymph originated at the deep posterior thoracic region, corresponding to the last five intercostal spaces.

There are two lymphatic ducts: the right lymphatic duct and the thoracic duct.

The first is formed by the confluence of the right jugular trunk, right subclavian trunk, and right bronchomediastinal trunk; generally, this duct empties into the right jugulosubclavian confluence.

The thoracic duct is originated from the descending intercostal trunks, the right and left lumbar trunks, and the gastrointestinal trunk. Cisterna chyli is an ampular dilatation frequently observed where those trunks meet and is located between the azygous vein and aorta at the level of L2 to D12. Just after its origin, the thoracic duct runs cranially through the aortic hiatus of the diaphragm, to the right of the median sagittal plane, and around D5 level it turns to the left side, crossing the

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Figure 1. Anterior view of the upper limb. Schematic distribution of the superficial bundles of the forearm and arm. Observe the epitroclear lymph node

posterior aspect of the thoracic esophagus. At the base of the neck, it reaches the left jugulosubclavian junction and near its terminal portion receives the left jugular, left subclavian, and left bronchomediastinal trunks.

Therefore, according to the lymphatic drainage, the body can be divided into four quadrants and all but the upper right quadrant are drained by the thoracic duct.

ANATOMY OF THE LYMPHATICS OF THE UPPER LIMBS

The lymphatic drainage of the superior limbs has two components: a superficial drainage and a less important one, the deep lymphatic system. Both systems anastomose and most of the upper limb lymph has a common final destination: the axillary lymph nodes. The superficial lymphatic system has ten bundles (Figs. 1 and 2), each one of them with one to many lymphatic collectors.Anastomoses between bundles are frequent.

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Figure 2. Posterior view of the superficial lymphatic bundles of the upper limb

Didactically, the bundles can be divided into six proximal bundles in the arm and four distal in the forearm and hand. The proximal bundles are further subdivided into three anterior and three posterior bundles (4).

Anterior bundles are, according to their drainage area, cephalic, basilic (Fig. 3), and prebicipital; and the posterior ones are posteromedial, posterior, and posterolateral.

The four bundles that drain the distal regions are divided into two anterior (anterior radial and anterior ulnar) and two posterior (posterior radial and posterior ulnar).

The deep lymphatic drainage of the upper arms has six bundles: two proximal in the arm and four distal.The proximal bundles are denominated brachial (Fig. 4) and deep brachial due to their anatomical relation witsh the homonymous arteries.

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Figure 3. Basilic bundle observed after intradermal injection of Gerota’s mass in the anterior aspect of the forearm. Impregnation of lymph nodes of the anterior and lateral lymph node groups of the axilla

The four distal comprise three anterior bundles: deep radial, deep ulnar, and anterior interosseal (Fig. 5), and one posterior: posterior interosseal (6–9) (Fig. 6).

Derivative pathways are lymph collectors that do not reach the expected drainage site at the root of the limbs. For the upper limbs, two different derivative pathways can be identified.They are the cephalic and the posterior bundles that run to the supraclavicular nodes and posterior scapular nodes, respectively.These derivative pathways are one of the possible explanations of why lymphedema does not always develop after axillary resection and radiation for breast cancer treatment (4).

Lymph nodes of the upper limbs can also be classified as superficial and deep (4).

Superficial lymph nodes are found in the arm (Fig. 1) accompanying the basilic vein, called epitroclear lymph nodes, and in the deltoideopectoral sulcus, called deltoideopectoral lymph nodes. Deep lymph nodes (Figs. 4–6) are located in the arm and in the forearm.Arm lymph nodes are found close to the vessels and are so denominated brachial and deep brachial lymph nodes. In the forearm, there are anterior lymph nodes (radial, ulnar, and anterior interosseal) and a posterior one (posterior interosseal) (6–9).

Lymph nodes in the axilla (Figs. 7–9) are organized as lymph centers or chains and receive lymph from the following regions: upper limb, supraumbilical area up to the clavicle, and dorsal region (10).These chains are classified according to their location in:

1. Anterior group (also pectoral or external mammary or lateral thoracic). Located at the infe- rior border of the pectoralis major muscle and related with the lateral thoracic artery.This chain receives lymph from most of the breast and supraumbilical region.

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Figure 4. Schematic anterior view of the deep bundles and lymph nodes of the arm and their relationship with the arteries

2. Posterior group (also subscapular). Situated anterior to the subscapular muscle, all along the subscapular vessels and receives lymph from the dorsum.

3. Lateral group (or axillary).This chain accompanies the axillary vessels, situated ante- rior, posterior, superior, and inferior to them and drains lymph from the upper limb, except the lymph that flows through derivative pathways.

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Figure 5. Anterior view of the deep bundles and lymph nodes of the forearm

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Figure 6. Anterior view of the deep bundles and lymph nodes of the arm, medial and posterior to the biceps muscle

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Figure 7. Lymph nodes of the axilla. The anterior group is related to the lateral thoracic artery and is fol- lowed by the lateral and posterior chains.The intermediate group receives afferent vessels from the previous groups. Medial or apical chain is located medial to the minor pectoralis muscle

Figure 8. Basilic bundle and lateral lymph nodes of the axilla after injection in the hand

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Figure 9. Lymphatic drainage of the breast to the lymph nodes of the axilla and internal mammary chain

4. Intermediate group (or central).This is also located following the axillary vessels but is immediately medial to the previous group, receiving lymph from efferent vessels of the lateral chain.

5. Medial group (or apical). This last group is situated medial to the pectoralis minor muscle, receives efferent vessels from the intermediate group and from this group, efferent vessels form the subclavian trunk that flows to the lymphatic duct on the right side and thoracic duct on the left.

ANATOMY OF THE LYMPHATICS OF THE LOWER LIMBS

The lymphatic drainage of the lower limbs also consists of two different systems:

the deep and the superficial system (2).

The superficial system has six different bundles (11) (Figs. 10–12), two distal in the foot and in the leg, named according to the main vein they follow: great saphenous bundle (or ventromedial) and lesser saphenous (or posterolateral) bundle. The other four proximal bundles are located in the thigh and are subsequently divided in two anterior and two posterior bundles.The anterior bundles are the anteromedial of the thigh (or ventromedial or great saphenous bundle) and anterolateral of the thigh.The posterior bundles of the thigh are denominated posteromedial and posterolateral.

The great saphenous bundle of the leg extends upward and continues as the anteromedial bundle of the thigh.These lymphatic vessels converge posterior to the medial condilum of the femur to reach the thigh. The great saphenous bundle of

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Figure 10. Anterior view of the lower limb. Schematic distribution of the superficial bundles of the leg and thigh. Observe that the accessory saphenous bundle is restricted to the thigh

the leg receives anastomotic vessels from the lesser saphenous bundle. The anterolateral bundle of the thigh, also called the accessory saphenous bundle, originates in the thigh so there is no direct connection between this bundle and the lymphatics of the leg (5) (Fig. 10). It is also important to notice the close relationship between the great saphenous vein and the accompanying lymphatic bundle, especially in the

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Figure 11. Posterior view of the lower limb. Observe the superficial popliteal lymph node

knee area, which makes the latter susceptible to trauma in operations for saphenous harvest to aortocoronary bypass and some surgical procedures for varicose veins (2).

The deep lymphatic drainage of the lower limb has five lymphatic bundles, being three distal (leg and foot) and two proximal in the thigh.

The deep lymphatic bundles of the foot and leg are divided in one anterior (Fig. 13) and two posterior (Fig. 14). The anterior bundle is named anteromedial

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Figure 12. Superficial inguinal lymph nodes and their relationship with the branches of the great saphenous vein after injection in the foot

bundle or anterior tibial and the posterior ones are called posteromedial or posterior tibial, and the last one posterolateral or fibular bundle.

In the thigh, the deep lymphatic bundles accompany the femoral artery and the deep femoral artery (Fig. 15) and drain into the deep inguinal lymph nodes (6–9).

Lower limbs also have deep and superficial lymph nodes (3). Superficial lymph nodes are found in the subcutaneous of the inguinal (Figs. 13 and 15) and popliteal regions (Fig. 14). Inguinal lymph nodes are related to the superficial regional veins:

great saphenous, accessory lateral saphenous, superficial circumflex iliac, superficial epigastric, and external pudenda.

The superficial inguinal lymph nodes are named according to their anatomical relationship with the neighboring vein (Fig. 16). There are six superficial nodal chains: three of them are located inferiorly and contain one single node (great saphenous, lateral accessory saphenous, and intersaphenous) and the remaining three are cranial to the saphenofemoral junction, and usually multinodal (superficial circumflex iliac, superficial epigastric, and external pudenda).

Usually, the lymphatic drainage of the lower limbs reaches the inferior inguinal lymph nodes (great saphenous, lateral accessory saphenous, and intersaphenous), while superior ones receive lymph from infraumbilical abdominal area, gluteus, external genitalia, and part of the uterus.The major labia of pudendum have both homolateral and contralateral drainage (6–9) (Figs. 16 and 17).

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Figure 13. View of the anterior deep bundle and lymph node of the leg

Superficial inguinal lymph nodes, mainly the inferior nodes, can be severed dur- ing great saphenous vein stripping and dissections of the inguinal area, due to their relationship with saphenofemoral junction, which may lead to lymphatic blockage and edema of the lower limb.

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Figure 14. View of the posterior deep bundles of the leg accompanying the posterior tibial and fibular arteries

In the popliteal region, the superficial popliteal node is commonly unique and receives lymph from the posterolateral bundle of the leg (Fig. 18).

Concerning deep lymph nodes, they are located in the leg, popliteal, and inguinal regions.

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Figure 15. Superficial inguinal lymph nodes and superficial bundles of the lower limb and their relationship with the great saphenous vein

Deep leg lymph nodes are usually situated near to the origin of the arteries, thus anterior tibial, posterior tibial, and fibular, and they receive lymph from the leg and foot (11). Deep popliteal chain (Fig. 19) usually contains ten lymph nodes and has the following distribution, according to their position regarding the popliteal vessels: one is anterior to the popliteal artery (anterior popliteal or prearterial); the nine lymph nodes remaining are related to the popliteal vein. Of those, three are

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Figure 16. Superficial inguinal lymph nodes after injection in both feet and left major labium with masses of different colors. Lymphatic drainage of the genital area injected goes to both inguinal areas

Figure 17. Schematic distribution of the lymphatic drainage of the major labia of the pudendum

situated lateral to the vein and three are medial. They have the denomination of superior, median, and inferior in each side, considering their location related to the joint.The three deep posterior lymph nodes (retropopliteal) receive their denomination according to their position cranial or caudal to the lesser saphenous popliteal

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Figure 18. Superficial popliteal lymph node and posterolateral bundle of the leg after injection in the lateral aspect of the foot

junction as two suprasaphenous and one infrasaphenous (2, 3, 11).This entire group drains lymph from subfascial portions of the leg and foot and can also receive lymph from the superficial area through perforator vessels.

Deep inguinal lymph nodes are located medial to the femoral vein and deep to saphenous femoral junction. There are fewer nodes as compared to the superficial chain and one of them, always present, lays near to the lacunar ligament and is called

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Figure 19. Deep popliteal lymph nodes and their relationship with the popliteal vessels

Cloquet’s lymph node (2, 3). This chain receives lymph from efferent vessels that accompany the femoral artery and also from the superficial area.

After the inguinal lymph nodes, lymph of the lower limbs reaches external iliac and common iliac lymph nodes. Subsequently, it passes through lumbar aortic lymph nodes that form the lumbar trunks and finally drain into the thoracic duct.

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ANATOMY OF THE LYMPHATICS OF THE PELVIS

Pelvic lymph nodes receive their denomination according to their topographic relationship to the iliac vessels as external, internal, and common iliac lymph nodal chains (10).

The external iliac chain, which follows inguinal lymph nodes, is subdivided into lateral, intermediate, and medial.The lateral lymph nodes are located at the lateral aspect of the external iliac artery and are superficial to the psoas muscle. The intermediate chain is found between the artery and the vein, and its more cranial lymph node is found near the common iliac artery bifurcation and is closely related to the ureter.

Medial external iliac lymph nodes are found medial to the external iliac vein and near the obturator nerve. Its more caudal node has a close relationship with Cloquet’s node (2, 3).

The internal iliac chain lies near to the internal iliac artery and its branches and has parietal and visceral lymph nodes.

The parietal nodes are superior and inferior gluteal, lateral sacral, and obturators.

The visceral are lateral, anterior and posterior vesical, rectal, and uterine.As visceral internal iliac lymph nodes are closely related to the pelvic organs, they are usually the first to be reached by lymphatic metastasis.

The common iliac lymph chain is located along the homonymous artery, and medial, lateral, and intermediate lymph nodes can also be identified. The medial one is the most cranial of them and sometimes is included in the subaortic lymph nodes group.

Thorough comprehension of lymphatic vessels and nodes of the pelvis, particularly those of the uterus, is very important due to the incidence of uterine carcinoma.

Thus, the fundus and upper part of the uterine body drain through lymphatic vessels of the round ligament to the superficial inguinal lymph nodes. Laterally, on the superior region of the broad ligament, its lymphatic drainage follows that of the uterine tube and ovary, accompanying the ovarian vessels to the lumbar aortic chain. On the other hand, the lymphatic drainage of the inferior portion of the uterine body and neck goes mainly to the pelvic lymph nodes, external, internal, and even common. Because of this massive spread of the cervical lymph drainage, complete removal of pelvic lymph nodes is sometimes required for the treatment of cervical carcinoma.

ANATOMY OF THE LYMPHATICS OF THE ABDOMEN

Lymph node chains of the abdominal cavity are retroperitoneal and are divided into aortoceliac and aortolumbar, respectively, superior and inferior to the left renal vessels.The first will form the gastrointestinal trunk and the latter the lumbar trunks (10).

The celiac aortic lymph nodes have three different chains:

1. Left aortoceliac, located between the lateral aspect of the aorta and the left diaphragmatic pillar

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2. Right aortoceliac, between the right side of the aorta and the right diaphragmatic pillar

3. Anterior aortoceliac, near the superior mesenteric artery origin

These three chains receive lymph from the spleen, pancreas, abdominal esophagus, liver, gallbladder, stomach, small intestine, cecum, ascending colon, and proximal two-thirds of the transverse colon. Also, some vessels from the left colic flexure and distal third of the transverse colon drain to this chain.

Aortolumbar lymph nodes are divided into three groups: preaortic, left aortic or left lateral aortic, and right aortic. Some authors describe a posterior aortic chain, which we believe does not exist because aortic pulse against the vertebra could damage them.

The preaortic chain is located anterior to the abdominal aorta and its lymph nodes are around the inferior mesenteric artery origin up to the inferior aspect of the left renal artery. This chain receives efferent lymph vessels from the left colic flexure, distal third of the transverse colon, descending colon, sigmoid and most of the rectum. Therefore, the distal part of the transverse colon and the left flexure have double lymphatic drainage.

The left aortic chain is located between the lateral aspect of the aorta and the psoas muscle.This chain collects lymph from the kidney, suprarenal gland, left common iliac chain, testicle or ovary, uterine tube, left superior portion of the uterus, and deep layer of the abdominal wall.

The right aortic chain is divided into precaval, interaortocaval, laterocaval, and retrocaval.The precaval group is represented by lymph nodes situated from the origin of the inferior cava vein until the inferior border of the right renal vessels.The interaortocaval group is found between the inferior cava vein and abdominal aorta until the inferior border of the left renal vessels.The laterocaval group is situated to the right of the vein and the retrocaval group is found posterior to the cava, anterior to the psoas muscle. These four lymph nodal groups receive the lymphatic drainage from the kidney, suprarenal gland, testicle or ovary, uterine tube, superior and lateral portion of the uterus, deep layer of the abdominal wall, and right common iliac chain.

The aortolumbar chains join at the median line and the main efferent lymph vessels from either side form two lumbar trunks that join with the gastrointestinal trunk to form the thoracic duct.

ANATOMY OF THE LYMPHATICS OF THE HEAD AND NECK

The lymphatic drainage from the head is made through four pathways (10):

1. Anterior or facial vessels. It receives the drainage from the frontal area and anterior portion of the face, except for the chin and inferior lip (that drain to the submental lymph nodes) and subsequently drains to the submandibular lymph nodes.

2. Parotideal. It receives the lymphatic drainage from the lateral aspect of the face, including the eyelid, flowing to parotideal lymph nodes.

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3. Retroauricular. It receives lymph from the parietal and temporal areas and drains to the mastoid or retroauricular lymph nodes.

4. Occipital. It receives lymph from the occipital region and drains to the occipital lymph nodes.

Superficial cervical lymph nodes are distributed along the external jugular vein, superficial to the sternocleidomastoid muscle, and their efferent vessels reach the deep cervical lymph nodes.

Deep cervical lymph nodes accompany the internal jugular vein, beneath the sternocleidomastoid muscle; some of these lymph nodes run posteriorly together with the accessory nerve and others run downward along with the subclavian vessels.

One lymph node located deep to the posterior body of the digastric muscle is denominated jugulodigastric and another, located superiorly to the tendon of the omohyoid muscle, is called juguloomohyoid.

Efferent lymph vessels from submental, submandibular, parotideal, retromandibu- lar, and occipital reach the deep cervical lymph nodes (jugulodigastric), located cranial to the internal jugular vein. The jugular trunk is formed by lymphatic vessels coming from deep cervical lymph nodes and flows to the thoracic duct on the right and to the thoracic duct on the left (10, 14).

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