2 Venous Embryology and Anatomy GEZA MOZES and PETER GLOVICZKI
tines. The right umbilical vein regresses completely, the left drains the placenta.3,4 The anterior cardinal veins drain the cranial part of the embryo and are connected to each other by a large central anastomosing channel. The segment of the left anterior cardinal vein located proximal to the anastomosis will regress. The oblique vein of the left atrium and the coronary sinus develop from the regressed proximal segment of the left anterior cardinal vein. The remaining distal segment becomes the left internal jugular vein and the anastomosis between the anterior cardinal veins forms the left brachiocephalic vein. The right internal jugular and brachiocephalic veins develop from the proximal segment of the right anterior cardinal vein. The external jugular veins develop secondarily. Failure of the regression of the proximal left anterior cardinal vein results in double superior vena cava (SVC), whereas erroneous regression on the right side results in left-sided SVC (see Figure 2.2a, b). The posterior cardinal veins run caudal to the heart and distally develop an interconnecting iliac anastomosis. Contrary to their anterior counterparts, the posterior cardinal veins regress almost completely. Only a small proximal segment remains on the right side to form the azygos arch and the iliac anastomosis to transform into the common, external, and internal iliac and median sacral veins. Most veins, caudal to the heart, develop from the sub- and supracardinal veins, which arise dorsal and ventral to the regressed posterior cardinal veins, respectively. The subcardinal veins anastomose with each other (subcardinal anastomosis) and with the supracardinal veins (subsupracardinal anastomosis). The majority of the left-sided cardinal veins regress. The right subcardinal vein develops to drain most of the upper, the right supracardinal vein most of the lower part of the abdomen.
INTRODUCTION Substantial knowledge has accumulated in recent years on development and anatomy of the venous system. Progress in medical genetics resulted in identification of genes linked to development of circulation and in recognition of growth factors affecting normal and abnormal development of blood vessels. Perfection of ultrasound technology combined with an increasing clinical interest in venous disease resulted in identification of new compartments and clinically important anatomic structures.1 Finally, a new, clinically relevant anatomic terminology of the veins of the leg and pelvis was introduced.2 In this chapter we discuss the embryology of the venous system and present the most frequent venous anomalies. We describe the histology of large veins and present a detailed anatomy of the veins of the trunk and the upper and lower limbs. Discussion of the anatomy of the visceral and cervical veins is beyond the scope of this review. The new terminology of veins will be used in this manuscript (see Table 2.1).
EMBRYOLOGY During embryogenesis the earliest veins develop from capillary plexuses; these carry blood into the sinus venosus, the in-flow end of the forming heart. The right and left common cardinal veins drain directly into the sinus venosus (see Figure 2.1). The common cardinal veins form at the junction of the anterior and posterior cardinal veins on both sides. Between this junction and the heart the common cardinal veins receive the vitelline and umbilical veins. The vitelline veins initially drain the yolk sac and later the intes-
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Chapter 2/Venous Embryology and Anatomy
Majority of the azygos system develops from the cranial part of the supracardinal veins. The infrarenal segment of the inferior vena cava (IVC) develops from the caudal right supracardinal vein. The renal segment of the IVC arises from the subsupracardinal anastomosis, a venous network
TABLE 2.1 Historic and New Anatomic Terms of Lower Extremity Veins Historic term Greater or long saphenous vein Smaller or short saphenous vein Saphenofemoral junction Giacomini’s vein Posterior arch vein or Leonardo’s vein Superficial femoral vein Cockett perforators (I,II,II) Boyd’s perforator Sherman’s perforators 24 cm perforators Hunter’s and Dodd’s perforators May’s or Kuster’s perforators
New term Great saphenous vein (GSV) Small saphenous vein (SSV) Confluence of the superficial inguinal veins Intersaphenous vein Posterior accessory great saphenous vein of the leg Femoral vein Posterior tibial perforators (lower, middle, upper) Paratibial perforator (proximal) Paratibial perforators Paratibial perforators Perforators of the femoral canal Ankle perforators
located circumferentially around the aorta (renal collar). Eventually, the posterior segment of the collar regresses and the anterior part gives the left renal vein. Most of the suprarenal segment of the IVC develops from the right subcardinal vein, except for the short hepatic segment, which originates directly from hepatic sinusoids.5 Variation in the complex development of IVC and left renal vein is not uncommon. If the right subcardinal vein fails to connect to the liver sinusoids, the suprarenal segment of the IVC will not develop, consequently the lower part of the body will be drained through the azygos system and the liver will drain directly into the heart. Double IVC (0.2–3%) occurs due to the persistence of the left supracardinal vein, therefore it usually involves only the infrarenal segment (see Figure 2.2).6 Left-sided IVC (<0.5%) develops if persistence of the left supracardinal vein is associated with regression of the right supracardinal vein (see Figure 2.2).7 Developmental variations of the left renal vein include persistent (circumaortic) renal collar (1–9%) and retroaortic left renal vein (1–2%) (see Figure 2.3).8 Capillaries of the primitive limb buds initially drain into the marginal sinuses. In the arm the ulnar portion of the marginal sinuses dominate over the radial ones, and eventually form the basilic, axillary, and subclavian veins. The
FIGURE 2.1 Embryology of the major veins (adopted from Avery LB. Developmental Anatomy, revised 7th ed. Philadelphia: WB Saunders, 1974).
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Anatomy of the Thoracic Veins
subclavian vein drains into the proximal anterior cardinal vein. The cephalic vein develops secondarily from segments of the radial marginal sinuses and attaches to the axillary vein later. In the leg, segments of the primitive marginal sinuses persist only distally and develop into the peroneal, anterior tibial, and small saphenous veins. The great saphenous vein originates from the posterior cardinal vein and later gives off the femoral, popliteal, and posterior tibial veins.
FIGURE 2.2 Developmental anomalies of the superior (SVC) and inferior vena cava (IVC). a. Double SVC (posterior view). b. Left SVC (posterior view). c. Double IVC. d. Left IVC.
The venous wall has three layers: intima, media, and adventitia. The intima is made up by endothelial cells and an underlying thin connective tissue layer. Valves are formed by infolding of the intima, therefore they are covered with endothelium on both sides and have a very thin connective tissue skeleton. Venous valves are bicuspid. The veins are distended at the base of the valves, probably secondary to the effects of local flow reversal. The border of the intima is marked by the internal elastic lamina: a layer of thick elastic fibers. The internal elastic lamina is well developed only in large veins; it is incomplete in medium-sized and absent in small ones. The media is composed of smooth muscle cells and connective tissue fibers, most of which is collagen. Larger superficial veins, such as the GSV, have thick muscular media with the ability of significant contraction. Smaller tributaries of the GSV have thinner media, and therefore are more prone to varicosity. Media of the deep calf veins contain plenty of collagen, providing better wall strength. More central deep veins, such as femoral, iliac, axillary, and subclavian veins, contain less and less smooth muscle cell. The media of the superior and inferior vena cava is built up almost exclusively from connective tissue. The adventitia is poorly differentiated from the media, in particular in larger veins. It consists of some loose connective tissue with vasa vasorum and nerve fibers.9,10
ANATOMY OF THE THORACIC VEINS
FIGURE 2.3 Circumaortic renal collar.
The superior vena cava (SVC) starts at the confluence of the brachiocephalic veins behind the first right costal cartilage, and ends at the level of the third right costal cartilage where it drains into the right atrium. The SVC is about 7 cm long and 2 cm wide. Halfway along its course, before it enters the pericardium, the SVC receives the azygos arch. The brachiocephalic veins are formed at the confluence of the subclavian and internal jugular veins behind the sternoclavicular joints (see Figure 2.4). The right brachiocephalic vein is short, about 2–3 cm, and lies anterior to the innominate artery.7 The left one is about 6 cm long and courses obliquely behind the manubrium from left to right, anterior
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gives the entire right arm of the H, the hemiazygos gives the left lower and the accesory hemiazygos vein the left upper segment. The azygos vein starts at T12 to L2 with the confluence of the right ascending lumbar and subcostal veins. The azygos vein ascends on the right side up to the level of T4, then passes anterior to form an arch joining the SVC. Major tributaries of the azygos vein are the right posterior fifth to eleventh intercostal veins and the right superior intercostal vein draining the second to fourth intercostal veins. The hemiazygos vein starts similar to the azygos vein but on the left side of the vertebral column at T12–L2. It courses cranial and at the level of T8 it crosses over to join the azygos vein. Major tributaries of the hemiazygos vein are the left posterior eighth to eleventh intercostal veins. The accessory hemiazygos vein has more variation than the azygos and hemiazygos veins. Usually it drains the left superior intercostal vein (which in turn drains the left second to fourth intercostal veins) and the left posterior fifth to seventh intercostal veins. At the level of T7 it either crosses over to the right and joins the azygos or stays on the left and joins the hemiazygos vein. If the connection between the accessory hemiazygos and the rest of the azygoshemiazygos system is not developed, the accessory hemiazygos vein will drain through the left superior intercostal vein into the left brachiocephalic vein. The azygoshemiazygos system receives several small veins from the viscera of the chest and freely anastomoses with the vertebral venous plexuses as well. The azygos-hemiazygos system provides an important collateral pathway in case of IVC or SVC obstruction.7
ANATOMY OF THE UPPER EXTREMITY VEINS
FIGURE 2.4 Thoracic and retroperitoneal veins.
to the left subclavian, common carotid arteries, and superior to the aortic arch. Major tributaries of the brachiocephalic veins are the vertebral, internal thoracic, and inferior thyroid veins. The first intercostal vein drains into the brachiocephalic veins on both sides. The left superior intercostal vein is connected to the left brachiocephalic vein, whereas on the right it joins the azygos vein. There are no valves in either the SVC or the brachiocephalic veins. The azygos-hemiazygos system forms an H-shaped network in the posterior mediastinum, anterior to the body of the thoracic vertebrae (see Figure 2.4). The azygos vein
The dorsal and palmar digital veins join to form the metacarpal veins, which drain into the superficially located dorsal venous network of the hand. The cephalic and basilic veins arise from this network on the radial and ulnar side of the wrist, respectively. The superficial veins on the palmar side of the hand are richly anastomosed to the deep veins. A superficial and a more proximal deep venous arch is formed from the interconnection of the palmar veins and parallel the corresponding arterial arches. The cephalic vein originates at the anatomical snuff box from the dorsal venous network. It courses over the distal radius to the ventral aspect of the forearm and ascends on the lateral side of the arm. The cephalic vein runs in the deltopectoral groove, it enters the infraclavicular fossa behind the pectoralis major muscle and pierces the clavipectoral fascia before empting into the axillary vein (see Figure 2.5). The basilic vein begins on the ulnar side of the wrist, passes along the ulnar aspect of the forearm, and courses more ventrally at the level of the elbow. Above the elbow
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Anatomy of the Abdominal and Pelvic Veins
sponding arteries. The three pairs of deep veins of the forearm form the brachial veins at the level of the elbow. The paired brachial veins join the basilic vein to form the axillary vein at the lower border of the teres major muscle (at the lateral border of the scapula on an antero-posterior chest x-ray). The axillary vein is located medial and inferior to the axillary artery and the medial cord of the brachial plexus lies between the two vessels. The axillary vein ends at the outer border of the first rib where it becomes the subclavian vein. The subclavian vein runs posterior and superior to the subclavian artery and recives its only major tributary, the external jugular vein. The subclavian vein ends at the medial border of the scalenus anterior muscle where it joins the internal jugular vein to form the brachiocephalic vein. There are valves in the superficial and deep veins of the arm, although they are not so numerous as in the leg. Valves in the axillary vein usually are located proximal to the junction with the brachial and cephalic veins. The subclavian vein has a valve just proximal to the confluence of the external jugular vein. Upper extremity venous return is maintained mainly by the work of the heart without significant contribution of a muscle pump. Therefore the valves are less important from a functional standpoint. Perforators between the deep and superficial veins are scarce.
ANATOMY OF THE ABDOMINAL AND PELVIC VEINS
FIGURE 2.5 Upper extremity superficial veins.
the basilic vein runs medial to the biceps and at about midway in the upper arm it perforates the deep fascia and joins the brachial vein. After receiving the brachial vein, the basilic vein continues in the axillary vein. The median cubital vein connects the cephalic and basilic veins in the antecubital fossa. The medial antebrachial vein originates from the superficial palmar venous plexus and runs on the ventral side of the forearm. It joins either the cephalic or basilic vein or both in the proximal forearm. The accessory cephalic vein originates from the dorsal venous plexus on the ulnar side and crosses over dorsally to join the cephalic vein in the forearm. Variations in the anatomy of superfical arm veins are countless. Deep veins of the hand join to form the paired radial, ulnar, and interosseus veins, which accompany the corre-
The inferior vena cava (IVC) begins at the confluence of the common iliac veins and ascends on the right side of the vertebral column, passes through the tendinous portion of the diaphragm, and after a short course (approximately 2.5 cm) in the chest it terminates in the right atrium at the level of T9. In the upper abdomen the IVC is located posterior to the duodenum, the head and neck of the pancreas, the lesser sac, and the liver. The intrahepatic portion of the IVC lies in a groove along the posterior aspect of the caudate lobe. Tributaries of the IVC are the paired lumbar and renal veins and the hepatic veins, additionally on the right side the right gonadal, suprarenal, and inferior phrenic veins also drain into the IVC (see Figure 2.4). The left gonadal and suprarenal veins join the left renal vein, the left inferior phrenic vein drains into the left suprarenal vein. In case of IVC obstruction, communication between the veins of the thoracic and abdominal wall (thoracoepigastric, internal thoracic, and epigastric veins), the lumbar-azygos anastomosis, and the vertebral plexuses provide important collateral pathways. The common iliac veins begin at the sacroiliac joint on both sides and end at L5, where they form the IVC. The only tributary of the right common iliac vein is the right ascending lumbar vein; the left common iliac vein drains the left ascending lumbar and median sacral veins (see Figure 2.4).
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FIGURE 2.6 Relationship between the fascia and veins of the lower extremity. The fascia covers the muscle and separates the deep from the superficial compartment. Superficial veins (a) drain the subpapillary and reticular venous plexuses, and are connected to deep veins through perforating veins (b). The saphenous fascia invests the saphenous vein. The saphenous compartment is a subcompartment of the superficial compartment.
The right common iliac vein lies postero-lateral to the right common iliac artery. The distal segment of the left common iliac vein is medial and posterior to the left common iliac artery, the proximal segment is posterior to the right iliac artery and distal aorta. Compression of the proximal left common iliac vein may occur due to the overlying arterial structures. The external iliac vein starts at the level of the inguinal ligament, it courses along the pelvic brim and ends anterior to the sacroiliac joint where the external and internal iliac veins form the common iliac vein. On the right the distal external iliac vein is medial to the artery; however, as it ascends, more proximally, it courses posterior to it. The left external iliac vein remains medial to the artery along its entire course. Tributaries of the external iliac vein are the inferior epigastric, deep circumflex iliac, and pubic veins. The internal iliac vein runs postero-medial to the internal iliac artery on both sides. The short trunk of internal iliac vein is formed by the confluence of extra and intrapelvic venous tributaries. The extrapelvic tributaries include the gluteal (superior and inferior), internal pudendal, and obturator veins, which drain the pelvic wall and the perineum. Intrapelvic tributaries of the internal iliac vein are the lateral sacral and visceral (middle rectal, vesical, uterine, and vaginal) veins, which drain the presacral and pelvic visceral venous plexuses (rectal, vesical, prostatic, uterine, and vaginal). Both the IVC and the common iliac veins are valveless. There is usually one valve in the external iliac vein, however often it is without any valves.
ANATOMY OF THE LOWER EXTREMITY VEINS Thorough knowledge of the fascial compartments of the leg is a prerequisite of understanding the relationship between superficial and deep veins. The fascia surrounding the calf and thigh muscles separates two compartments: the superficial compartment, consisting of all tissues between the skin and the fascia, and the deep compartment, which includes all tissues between the fascia and the bones (see Figure 2.6).11 Superficial veins run in the superfical, deep veins in the deep compartments. Perforating veins pierce through the fascia and connect the superficial to deep veins.12 Communicating veins connect veins within the same compartment: superficial to superficial or deep to deep veins. The saphenous veins are covered by a fibrous sheath, the saphenous fascia. The saphenous fascia is thinner than the deep fascia and it is more pronounced in the upper-mid thigh, than more distally.1,13 The space between the saphenous and muscular deep fascia is the saphenous compartment. The saphenous compartment is a subcompartment of the superficial compartment. The superficial venous system of the foot is divided into the dorsal and plantar subcutaneous venous network (see Figure 2.7). Superficial vein tributaries drain blood into the dorsal venous arch on the dorsum of the foot at the level of the proximal head of the metatarsal bones. The medial and lateral end of this arch continues through the medial and
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Anatomy of the Lower Extremity Veins
FIGURE 2.7 Superficial and perforating veins of the foot and ankle.
lateral marginal vein into the great (GSV) and small saphenous veins (SSV), respectively. Small superficial veins drain the subpapillary and reticular plexuses of the skin and subcutaneous tissues to form bigger tributaries, which eventually all connect to the saphenous veins.14,15 The GSV begins just anterior to the medial ankle, crosses in front of the tibia, and ascends medial to the knee (see Figure 2.8).16–18 Proximal to the knee, the GSV ascends on the medial side of the thigh and enters the fossa ovalis 3 cm inferior and 3 cm lateral to the pubic tubercle.19 The GSV is doubled in the calf in 25% of the population, in the thigh in 8%.20 The saphenous nerve runs in close proximity to the GSV in the distal two-thirds of the calf. Accessory great saphenous veins are frequently present and they run parallel to the GSV both in the thigh and in the leg; they lie either anterior, posterior, or superficial to the main trunk. The posterior accessory GSV of the leg (Leonardo’s vein or posterior arch vein) is a common tributary, it begins posterior to the medial malleolus, ascends on the posteromedial aspect of the calf, and joins the GSV distal to the knee (see Figure 2.8). The anterior accessory GSV of the leg drains the anterior aspect of the leg below the knee. The posterior accessory GCV of the thigh, if present, drains the medial and posterior thigh.11 The anterior accessory GSV of the thigh collects blood from the anterior and lateral side of the thigh (see Figure 2.8). The anterior and posterior accessory GSVs join the GSV just before it ends at the confluence of superficial inguinal veins (saphenofemoral junction). The superficial circumflex iliac, superficial epigastric, and exter-
FIGURE 2.8 Superficial and perforating veins of the leg.
nal pudendal veins join each other and the distal GSV to form the confluence of superficial inguinal veins (saphenofemoral junction) (see Figure 2.9).21 Rarely, the GSV terminates high on the lower abdomen or joins the femoral vein very low and the superficial inguinal veins empty individually into the femoral vein.22 Other occasional tributaries of the GSV in the groin include the posterior and anterior thigh circumflex veins. The small saphenous vein (SSV) lies lateral to the Achilles tendon in the distal calf (see Figure 2.10).23 In the lower two-thirds of the calf the SSV runs in the subcutaneous fat, then it pierces the fascia and runs between the two heads of the gastrocnemius muscle. In the popliteal fossa at about 5 cm proximal to the knee crease, the main trunk of the SSV drains into the popliteal vein. A smaller vein, the cranial extension of the SSV, frequently continues in cephalad direction (see Figure 2.10).24 Uncommonly the main trunk of the SSV continues without draining into the popliteal vein and eventually empties into the femoral vein or GSV.11 The intersaphenous vein (vein of Giacomini) is a communicating vein connecting the SSV to the GSV in the
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Chapter 2/Venous Embryology and Anatomy
FIGURE 2.9 Common variations (a. −33%, b. −15%, c. −15%, d. −13%) in the anatomy of the confluence of inguinal veins (saphenofemoral junction).
FIGURE 2.11 Deep veins of the foot and calf.
FIGURE 2.10 The small saphenous vein and lateral venous system of the calf.
posterior-medial thigh. The sural nerve courses along the SSV in the distal calf. Superficial veins of the lateral leg and thigh form the lateral venous system. The lateral venous system is drained through multiple small tributaries into the GSV and SSV. Deep veins of the foot form two divisions: the plantar and the dorsal veins. The richly anastomosing deep plantar venous arch drains the plantar digital veins through the plantar metatarsal veins. The deep plantar venous arch drains into the medial and lateral plantar veins, which in turn continue in the posterior tibial veins behind the medial ankle (see Figure 2.11).25 On the dorsum of the foot the pedal vein drains the deep dorsal digital veins through the dorsal metatarsal veins. The pedal vein continues in the anterior tibial veins. Pairs of the posterior and anterior tibial and peroneal veins accompany the corresponding arteries, and all drain into the popliteal vein (see Figures 2.11 and 2.12). Large soleal and gastrocnemius (medial, lateral, and intergemellar) veins drain venous sinuses of calf muscles and join the popliteal vein. Venous sinuses are closely related to deep veins. They are embedded in the belly of calf muscles, such
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Anatomy of the Lower Extremity Veins
as the soleus and gastrocnemius, and are able to dilate and hold a large amount of blood. With the contraction of calf muscles at walking the blood is pumped to more proximal deep veins (calf muscle pump). The popliteal vein continues into the femoral vein as it is passing through the adductor
FIGURE 2.12 Deep veins of the leg.
canal. The popliteal and femoral veins are frequently duplicated.26 Distally the femoral vein runs lateral to the femoral artery; however, more proximally it runs medial to it. The deep femoral (profunda femoris) vein joins the femoral vein to form the common femoral vein at about 9 cm below the inguinal ligament.27 The common femoral vein is medial to the common femoral artery and it becomes the external iliac vein at the level of the inguinal ligament. The GSV joins the common femoral vein at the confluence of the superficial inguinal veins. Other tributaries of the common femoral vein are the circumflex femoral veins (lateral and medial). In the distal thigh the femoro-popliteal segment frequently communicates through a large collateral with the deep femoral vein providing an important alternative avenue for venous drainage in case of femoral vein occlusion. The sciatic vein, the main trunk of the primordial deep venous system, runs along the sciatic nerve. There are as much as 150 perforating veins (PVs) in the lower extremity; however, only a few of these are clinically important. Significant variation exists in the location of individual PVs; however, distribution of clusters of PVs follows a predictable pattern. Dorsal, plantar, medial, and lateral foot perforators are the main groups of PVs in the foot.28 A large PV runs between the first and second metatarsal bones and connects the superficial dorsal venous arch to the pedal vein.29 Clusters of PVs at the ankle are the anterior, medial, and lateral ankle perforators (see Figure 2.13).30 The medial calf perforators have two groups: posterior tibial and paratibial PVs. Three groups (lower, middle, upper) of posterior tibial PVs (Cockett I–III perforators) connect the posterior accessory GSV to the posterior tibial veins (see Figures 2.8, 2.11, and 2.13).31,32 The paratibial perforators drain the GSV
FIGURE 2.13 Relationship of the posterior tibial perforators to the deep and superficial posterior compartments (SPC) of the calf (PTVs, posterior tibial veins).
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Chapter 2/Venous Embryology and Anatomy
into the posterior tibial veins.33,34 Other perforators of the leg below the knee are the anterior, lateral, medial, and lateral gastrocnemius; intergemellar and Achillean PVs (see Figure 2.11). Infra- and suprapatellar and popliteal fossa PVs are located around the knee. Perforators of the femoral canal connect tributaries of the GSV to the femoral vein (see Figure 2.8). Inguinal perforators drain into the femoral vein in the proximal thigh. Valves in superficial veins of the lower extremity usually are located near to the termination of major tributaries. Some valves are well developed with marked sinusoid dilation at their base, others are more delicate in their structure. In the GSV there are about six valves, with more valves located below than above the knee. A nearly constant valve of GSV is at 2–3 cm distal to its confluence with the femoral vein. Valves in the SSV are closer to each other than in the GSV. Valves in communicating branches between the SSV and GSV are oriented to direct blood from the small to the great saphenous vein. Similar to superficial veins, deep veins have more valves in the calf than in the thigh. Tibial veins are densely packed with valves, whereas there are only one or two valves in the popliteal vein. In the femoral vein there are three to five valves, with one of them located just distal to the junction of the deep femoral vein. There is usually one valve in the common femoral vein. Major PVs have one to three valves, all located below the level of the fascia, that direct flow toward the deep veins. Small PVs are usually valveless. PVs of the foot are without any valves or with valves that direct flow toward the superficial veins.
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