(1)
Department of Anatomy, Xuzhou Medical College, Xuzhou, Jiangsu, China
1 Lymphatic Valves
Since lymphatic vessels in the mesentery of the postprandial dog were originally discovered by Aselli(1627), the lymphatic valves were identified and their morphology and function were described by Ruysch (1665) and Lord (1967).
An existence of abundant lymphatic valves in most lymphatic vessels was confirmed by Cruikshank (1786), Mascagni (1787), Cooper (1840), and Sappey (1874) et al., prior to the discovery of X-rays in 1895 using a mercury injection, which was then recorded by a series of drawings.
After a new technique was established (Suami et al. 2005a), lymphatic valves could be observed under a surgical microscopy in human cadaver tissue and recorded by photographs and radiographs (Pan et al. 2010a, b and c).
1.1 Structure of Valves
The size of paired valves varied according to the calibre of the vessels, small in precollecting lymph vessels and large in lymphatic ducts. Each vessel segment (inter-valvular section) between valves formed a peanut-like fragment, the cusp (valves) of the distal side of the fragment inserted and opened into the blunt end of the proximal side of the segment, which formed a constrictive ring on the vessel wall (Fig. 2.1).
Fig. 2.1
(a) A longitudinal section of an afferent lymph vessel filled with lead oxide mixture showing the inner structure of the vessel. (b) The structures in the blue-circled area have been magnified showing the vessel walls (W) and valves (V) and the lumen of the vessel filled by lead oxide mixture (L). Green arrows indicate valves
1.2 Appearance of Valves
Multiple valves were present in the lumen of the precollecting and collecting lymph vessels, lymphatic trunks and lymphatic ducts. There were numerous valves in lymph-collecting vessels and trunks and sparse in lymph-precollecting vessels. Vessels looked like a string of beads or a bamboo trunk (Figs. 2.2, 2.3, 2.4, 2.5, 2.6, 2.7 and 2.8) depending on the ratio between the diameter of vessels and the interval length of the vessel in valves. Valves occurred at intervals averaging 2 mm (ranging from 1 to 3 mm) in the collecting lymph vessels and the lymphatic trunks. The diameter of the collecting lymph vessels averaged 0.2 mm (Figs. 2.2 and 2.4). The ratio of the diameter of the vessel and the interval length of valves is ≤0.1. Thus, most collecting lymph vessels resembled bamboo trunks (Fig. 2.7a, c). The diameter of the lymphatic trunks averaged 2 mm (Fig. 2.6). The ratio of the diameter of the vessels and the interval length of valves is ≥1; therefore, most lymphatic trunks look like a string of beads (Fig. 2.7b, d).
Fig. 2.2
An image showing precollecting (P) and collecting (C) lymph vessels filled with lead oxide mixture lying in the galea layer (G) of the parietal region. Green arrows indicate valves and red arrows indicate the direction of lymph flow. A single small ampulla (A) was presented
Fig. 2.3
An image showing the lymphatic capillary plexus (LCP) and precollecting lymph vessels (P) filled with India ink mixture lying in the galea layer of the occipital region. Green arrows indicate valves and red arrows indicate the direction of lymph flow
Fig. 2.4
Two collecting lymph vessels filled with lead oxide mixture in the preauricular area, different calibre and valves indicated by green arrows. Red arrows indicate the direction of lymph flow
Fig. 2.5
An internodal vessels filled with lead oxide mixture showing their calibre, number of valves (indicated by green arrows) and appearance. Red arrows indicate the direction of lymph flow. LN lymph node
Fig. 2.6
Lymphatic trunks in the supraclavicular region filled with lead oxide mixture showing calibre, valves and appearance. Valves were so numerous that this specimen resembled a “string of beads”. Green arrows indicate valves and red arrows indicate the direction of lymph flow
Fig. 2.7
Comparison of the appearance, calibre and inter-valvular section in the collecting lymph vessel and lymphatic trunk. Phtographs of the collecting lymph vessel (a) and the lymphatic trunks (b); Line drawings of the collecting lymph vessel (c) and lymphatic trunk (d)
Fig. 2.8
Radiological manifestations of valves of collecting lymph vessels in the subcutaneous of the thigh
1.3 Abnormal Valves
Usually lymphatic valves were presented in pairs in the lumen of the lymph vessels, but abnormal valves were found occasionally (Figs. 2.9 and 2.10).
Fig. 2.9
Multiple lymphatic valves (MV)
Fig. 2.10
Two-way lymphatic valves. A photograph of the collecting lymph vessel (a) and a line drawing of the same vessel (b)
Clinical Implication
The characteristic appearances of a string of beads or a bamboo trunk of the lymphatic vessels were related to the vessels’ calibre and inter-valvular section in the collecting lymph vessel (and lymphatic trunk). These descriptions may help surgeons distinguish the lymphatic vessels from the venula during lymphaticovenous anastomoses when treating secondary lymphoedema.
The lymphatic flap (pedicle or free) transfer is a surgical procedure to treat secondary lymphoedema (Becker and Hidden 1988). Due to lymphatic valves opened centripetally, the direction of lymph flow in the flap and the recipient site should be consistent during the procedure (Gillies 1935).
2 Lymphatic Ampullae and Diverticula
Different sizes and shapes of dilated vascular structures, lymphatic ampullae (Figs. 2.2, 2.11, 2.12, 2.13, 2.14, 2.15, 2.16, 2.17, 2.18, 2.19, 2.20, 2.21, 2.22, 2.23, 2.24, 2.25, 2.26, 2.27, 2.28, 2.29, 2.30 and 2.31) and diverticula (Figs. 2.32, 2.33, 2.34, 2.35, 2.36, 2.37, 2.38, 2.39, 2.40, 2.41, 2.42, 2.43, 2.44, 2.45 and 2.46) were found along the lymphatic pathway. They appeared singularly or in paired structures and circular or irregular in shape. Histological analysis confirmed that these structures had hollow centres filled with lead oxide (Fig. 2.13). Their origin and purpose are unknown.
2.1 Lymphatic Ampullae
Fig. 2.11
Gourd-shaped lymphatic ampulla structures (A), filled with lead oxide mixture, found in a collecting lymph vessel in the occipital region. Red arrows indicated the direction of lymphatic flow
Fig. 2.12
A radiograph showing the lymphatic vessels in the integument of the head and neck after lead oxide mixture injection. The area boxed blue is the site of vessels with ampulla structures. A magnified image of the area boxed blue showed in Fig. 2.13
Fig. 2.13
(a) Magnified vessel from Fig. 2.12. (b) Magnified lymphatic ampullae filled with lead oxide mixture and (c) histological sections of each type found on this vessel
Fig. 2.14
Different sized and shaped lymphatic ampulla structures (A) filled with lead oxide mixture in the retroauricular region. Red arrows indicate the direction of lymphatic flow
Fig. 2.15
A single ball-shaped lymphatic ampulla (A) filled with lead oxide mixture found in a lymphatic vessel of the cheek
Fig. 2.16
A single ball-shaped lymphatic ampulla (A) found in a lymphatic vessel of the earlobe
Fig. 2.17
A single oval-shaped lymphatic ampulla (A) seen in a collecting lymph vessel found in the preauricular area
Fig. 2.18
A single oval-shaped lymphatic ampulla (A) seen in a collecting lymph vessel found in the subauricular region
Fig. 2.19
A lymphatic ampulla (A) seen in the precollecting lymph vessel (P) filled with lead oxide mixture in the scalp. LCP lymph capillary plexus, C collecting lymph vessel
Fig. 2.20
A lymphatic ampulla (A) and precollecting lymph vessels (P) distended with hydrogen peroxide in the mucosa (M) of the root of the tongue
Fig. 2.21
Two lymphatic ampullae (A) seen in collecting lymph vessels distended by hydrogen peroxide mixed with ink in the lateral side of the index finger
Fig. 2.22
A lymphatic ampulla (A) seen in the collecting lymph vessel filled with lead oxide mixture in the dorsum of the hand
Fig. 2.23
A lymphatic ampulla (A) seen in collecting lymph vessels filled with lead oxide mixture in the ventral forearm
Fig. 2.24
A lymphatic ampulla (A) seen in the collecting lymph vessel filled with lead oxide mixture in the dorsal forearm
Fig. 2.25
Two lymphatic ampullae (A) seen in collecting lymph vessels filled with lead oxide mixture in the medial side of the ankle
Fig. 2.26
A lymphatic ampulla (A) seen in a collecting lymph vessel on the medial side of the right foot
Fig. 2.27
A single oval-shaped lymphatic ampulla (A) seen in a collecting lymph vessel on the dorsum of the foot
Fig. 2.28
A lymphatic ampulla (A) seen in a collecting lymph vessel on lateral side of the foot
Fig. 2.29
Lymphatic ampullae (A) seen in collecting lymph vessels on the medial side of the left leg
Fig. 2.30
A lymphatic ampulla (A) seen in a collecting lymph vessel on the medial side of the left thigh. GSV great saphenous vein
Fig. 2.31
Lymphatic ampulla (A) seen in a collecting lymph vessel on the medial side of the right thigh. FA femoral artery, FV femoral vein
2.2 Lymphatic Diverticula
Fig. 2.32
A lymphatic diverticulum (D) and a lymph node (LN) seen in multiple collecting lymph vessels in the retroauricular region. Red arrows indicate the direction of the lymph flow
Fig. 2.33
A single diverticulum (D) situated on the wall of the afferent vessel near to the lymph node (LN) in the occipital region
Fig. 2.34
Two pairs of different size of diverticula (D) filled with lead oxide mixture in the submental area. Red arrows indicate the direction of the lymph flow
Fig. 2.35
A diverticulum (D) filled with lead oxide mixture in the dorsum of the left hand. Red arrows indicate the direction of the lymph flow. V metacarpal vein
Fig. 2.36
A lymphatic diverticulum (D) seen on the collecting lymph vessel in the dorsoulnar aspect of the hand. Red arrows indicate the direction of the lymph flow
Fig. 2.37
A single diverticulum (D) situated on the wall of the collecting vessel in the ventral forearm
Fig. 2.38
A diverticulum (D) situated on the wall of the collecting vessel in the subcutaneous of the dorsal forearm
Fig. 2.39
A diverticulum (D) situated on the wall of the collecting vessel in the subcutaneous of the medial dorsum of the foot
Fig. 2.40
A diverticulum (D) situated on the wall of the collecting vessel in the subcutaneous tissue below the medial malleolus area
Fig. 2.41
A diverticulum (D) situated on the wall of the collecting vessel in the subcutaneous tissue of the anterior aspect of the leg
Fig. 2.42
Multiple diverticula (D) situated on the wall of the collecting vessel in the subcutaneous tissue of the anteromedial aspect of the leg
Fig. 2.43
Two diverticula (D) situated on the wall of the collecting vessel in the subcutaneous tissue of the medial aspect of the leg
Fig. 2.44
A diverticulum (D) situated on the wall of the collecting vessel in the subcutaneous tissue of the medial aspect of the leg
Fig. 2.45
A diverticulum (D) situated on the wall of the collecting vessel in the subcutaneous tissue of the lateral aspect of the leg
Fig. 2.46
Multiple diverticula (D) situated on the wall of the collecting vessel in the subcutaneous tissue of the posterolateral aspect of the leg
Note
Ampullae and diverticula were found in all subjects at various stages of the lymphatic pathway, either in precollecting or collecting lymph vessels. Their origin and purpose are unknown.
3 Lymph Capillary Plexus
The lymph capillaries have been described in many textbooks to exist in most tissues and organs of the body except the epithelia, cartilage, cornea, etc. Those originating from the dermis and the mucous membranes have an important role in the immune defence mechanism, which has been well described (Drinker and Yoffey 1941; Cowdry 1950). Those found in the galea layer (Pan et al. 2008a, b) may have a similar role to those in the skin of the scalp, as the scalp is a common site of trauma.
It has been noticed that there are two layers of lymph capillaries, one superficial and one deeper, in the dermis (Fig. 1.3) (Hudack and McMaster 1933) and mucosa (Fig. 2.64). They connect to each other to form a three-dimensional network – the lymph capillary plexus. The diameter of these vessels varies; they are tiny in the superficial layer (less than 0.02 mm) and slightly larger in the deeper layer. Sometimes larger vessels, diameter greater than 0.2 mm, could be seen in the galea layer and mucosa (Figs. 2.52, 2.63 and 2.64).
These vessels were thin walled, irregularly shaped and very fragile. Sometimes they appeared constricted and at other times dilated. They branch abundantly and undergo anastomosis freely to form a rich avalvular plexus. The micromorphology of these vessels varied in different regions (Figs. 2.47, 2.48, 2.49, 2.50, 2.51, 2.52, 2.53, 2.54, 2.55, 2.56, 2.57, 2.58, 2.59, 2.60, 2.61, 2.62, 2.63, 2.64 and 2.65).
3.1 Lymph Capillary Plexus in the Skin (Dermis) of the Scalp
Fig. 2.47
The lymph capillary plexus in the dermis of the scalp filled with India ink and hydrogen peroxide mixture
Lymph capillary vessels were seen without valves in the skin (dermis) of the scalp. They form a very fine three-dimensional, polygonal network. The calibre of the vessels varied from as small as 0.02 to 0.15 mm, tiny in the superficial layer and slightly larger in the deeper (Figs. 2.19, 2.47, 2.48, 2.49, 2.50 and 2.51).
Fig. 2.48
(a) Two patches of the lymph capillary plexus in the dermis of the scalp retrogradely filled with lead oxide mixture. (b, c) Magnified views of patches from (a)
Fig. 2.49
(a) The lymph capillary plexus in the dermis of the scalp retrogradely filled with lead oxide mixture. Viewed skin side up. (b) Magnified image of the area circled above, showing different sized vessels, irregular and jagged walls
Fig. 2.50
(a) Transilluminated view of the injected lymphatics from the inner surface of the scalp. (b) The diagram is traced from the image above. Note: The lymph capillary plexus links to the precollecting lymph vessels that drain to collecting lymph vessels. Swollen structures on the precollecting vessels have been named as “ampullae”. Red arrows indicate the direction of the lymph flow
Fig. 2.51
(a) Transilluminated view of the injected lymphatics from the inner surface of the scalp. (b) The diagram is traced from the image above. The lymph capillary plexus links to the precollecting lymph vessels and then flows into the collecting lymph vessels. Swollen structure on the precollecting vessel is the “ampulla”
Clinical Implication
Erysipelas is a type of skin infection involving the lymph capillary plexus in dermis. It is most often caused by β-haemolytic streptococci and occurs most frequently on legs and the face. With a rapid onset, affected individuals typically develop symptoms including high fevers, chills, shaking, headaches, vomiting, malaise and general illness. The affected skin area is characterized clinically by shiny, swollen, warm, raised and tender scarlet lesions with distinct margins (Zhang 1984; Hall and Hall 2009).
3.2 Lymph Capillary Plexus in the Galea (Epicranial Aponeurosis)
Avalvular lymph capillary vessels were present in the galea layer. They formed a fine three-dimensional polygonal plexus. The calibre of vessels varied from as tiny as 0.014–0.2 mm. The network merged to link precollecting lymph vessels and drained to the collecting lymph vessel in the deep tissues (Figs. 2.3, 2.52, 2.53 and 2.54).
Fig. 2.52
Different sized vessels with irregular walls of the lymph capillary plexus filled with India ink and hydrogen peroxide mixture in the galea layer of the scalp. Red arrow indicates the direction of the lymph flow
Fig. 2.53
The lymph capillary plexus filled with India ink and hydrogen peroxide mixture in the whitish galea layer of the scalp. The network merged to form different sized precollectors linking the lymph-collecting vessels lying in the yellowish subcutaneous tissue
Fig. 2.54
The lymph capillary plexus filled with lead oxide mixture in the whitish galea layer of the occipital area. Capillary vessels merged and formed two precollecting lymph vessels linking the collecting lymph vessels. Red arrows indicate the direction of the lymph flow. U indicates an unknown “mop-like” lymphatic structure lying between three afferent vessels (one precollecting, two collecting) and an efferent lymph-collecting vessel
Clinical Implication
Lymphatic capillary vessels are widely distributed in the body and have an important role in the immune defence mechanism, which has been well described (Drinker and Yoffey 1941; Cowdry 1950). Those found in the galea layer (Pan et al. 2008a, b) may have a similar role to those in the skin, as the scalp is a common site of trauma.
3.3 Lymph Capillary Plexus in the Auricle
Avalvular lymph capillary vessels were seen in the skin (dermis) of the auricle. They formed a fine three-dimensional, polygonal structure. The calibre of vessels varied from as small as 0.014 to 0.2 mm (Figs. 2.55 and 2.56).
Fig. 2.55
(a) Lymphatic vessels of the left auricle were filled with lead oxide mixture. Transilluminated (b) and radiological (c) images are the magnified view of the blue box from (a). Lymph capillary vessels, in the helix of the left auricle, merged and formed several precollecting lymph vessels linking the collecting lymph vessels. Red arrows indicate the direction of the lymph flow
Fig. 2.56
The lymph capillary plexus in the dermis of the dorsum of the left auricle lying above the lymph-collecting vessels. Red arrows indicate the direction of the lymph flow
Note
Bionic tissue engineering and 3D printing technologies of the experimental auricle cartilage have been reported (Cao et al. 1997; Mannoor et al. 2013). The success of such technologies will allow researchers to open the way to manufacture tissues and organs of the human body for replacement in the clinic. Detailed vasculature (Houseman et al. 2000) including the lymphatic vessels (Pan et al. 2011a, b) of the auricle will provide a theoretical basis for completing an entire ear when these technologies will have been fully established in the future.
3.4 Lymph Capillary Plexus in the Mucosa of the Nasal Cavity
Avalvular lymph capillary vessels were seen as small “tree-like” branches in the mucosa of the nasal cavity. The calibre of vessels varied from 0.01 to 0.2 mm (Fig. 2.57).
Fig. 2.57
(a) Lymph capillary plexus and precollecting lymph vessels filled with lead oxide mixture in the mucosa of turbinates of the nasal cavity. Red arrows indicate the direction of the lymph flow. A histological section (b), H&E stain, of the middle turbinate in the blue box of (a) showing the different sizes of the vessel at different depths. The right images are magnified views of the blue boxes from the left images
3.5 Lymph Capillary Plexus in the Mucosa of the Nasal Pharyngeal Wall
Avalvular lymph capillary vessels were presented as small loops and “tree-like” structures in the mucosa of the nasal pharyngeal wall. The calibre of vessels varied from 0.01 to 0.2 mm (Figs. 2.58 and 2.59).
Fig. 2.58
(a) The lymph capillary plexus and precollecting lymph vessels filled with lead oxide mixture in the mucosa of the lateral nasopharyngeal wall. (b) A magnified view of area circled in (a). Red arrows indicate the direction of the lymph flow
Fig. 2.59
The lymph capillary plexus in the mucosa of the lateral nasopharyngeal wall draining to the parapharyngeal space via a precollecting lymphatic vessel. Red arrow indicates the direction of lymph flow
3.6 Lymph Capillary Plexus in the Mucosa of the Soft Palate
Avalvular lymph capillary vessels were presented as small loops structure in the mucosa of the soft palate. The calibre of vessels varied from 0.01 to 0.1 mm (Fig. 2.60).
Fig. 2.60
The lymph capillary plexus linked to the precollecting lymphatic vessel in the mucosa of the soft palate. Red arrow indicates the direction of lymph flow
3.7 Lymph Capillary Plexus in the Mucosa of the Oropharyngeal, Laryngeal and Oesophageal Walls
The lymph capillary vessels were seen as a “coral-like” structure without valves in the mucosa of the oropharyngeal, laryngeal and oesophageal walls. The calibre of vessels varied from 0.01 to 0.2 mm (Figs. 2.61, 2.62, 2.63 and 2.64).
Fig. 2.61
(a) The “coral-like” lymph capillary plexus filled with lead oxide mixture circled blue in the mucosa of the oropharyngeal. (b) Magnified view of the structure
Fig. 2.62
(a) The “coral-like” lymph capillary plexus filled with lead oxide mixture circled blue in the mucosa of the pharyngeal. (b) Magnified view of the structure
Fig. 2.63
(a) The “coral-like” lymph capillary plexus filled with lead oxide mixture in the mucosa of the oesophagus (superior portion). (b) A magnified view of the structure boxed in (a)
Fig. 2.64
The lymph capillary plexus filled with lead oxide mixture in the mucosa of the oesophagus. Histological section shows the different sizes of the vessels at different depths of the mucosa
Clinical Implication
Distribution of the lymph capillary vessels in the mucosa is extremely rich. They situate in the entire layer of the mucosa in different sizes and a 3D multi-level reticular formation. Similar to those found in the dermis, they have an important role in the immune defence mechanism which has been described (Roitt et al. 2003).
3.8 Lymph Capillary Plexus in the Breast
Lymph capillary vessels were found without valves in the subareola. They formed a three-dimensional polygonal plexus. The calibre of the vessels varied from as tiny as 0.014 to 0.2 mm. Vessels merged to become precollecting vessels and drained towards the axilla via the collecting lymph vessel (Fig. 2.65).
Fig. 2.65
(a) The lymph capillary plexus filled with lead oxide mixture in the subareola. (b) A magnified view of the blue box in (a). Red arrow indicates the direction of lymph flow
3.9 Abnormal Lymph Capillary Plexus (Figs. 2.66 and 2.67)
Fig. 2.66
The lymph capillary plexus (U) filled with lead oxide mixture in the parietooccipital galea layer. Red arrow indicates the direction of lymph flow
Fig. 2.67
(a) The lymph capillary plexus (U) filled with iodine mixture in the dorsum of the foot. (b) A magnified view of area circled in (a). Red arrows indicate the direction of lymph flow
Clinical Implication
Abnormal lymph capillary plexus was rare during the lymphatic dissection. Two of them were found during the entire study. They were small in sizes. One was 1 × 5 mm in the parietooccipital galea layer; the other one was 4 × 6 mm in the dorsum of the foot. Tiny vessels assembled irregularly connecting to either precollecting or collecting lymph vessels (Figs. 2.66 and 2.67). They may occur by two reasons: (1) congenital malformation of lymphatic capillary vessels (asymptomatic lymphangioma?) (Strigel 1996) and (2) acquired due to trauma (Zhang 1984).
4 Precollecting Lymph Vessels
Precollecting lymph vessels were seen to connect the lymph capillary plexus and collecting lymph vessels. They arose from the deep side of the dermis, mucosa, galea layer, etc. They travelled from the superficial to the deeper layer of the subcutaneous tissue in an ascending, descending, horizontal or looping manner and then drained into the collecting lymph vessels (Figs. 1.2, 1.3, 2.68, 2.69 and 2.70). The diameter of the precollecting lymph vessels varied from 0.1 to 0.3 mm in size when distended. The vessels contain lymphatic valves at 1 to 3 mm intervals giving the walls an irregular appearance similar to that of the bamboo trunk (Fig. 2.7).
In the scalp, two types of precollecting pathways were found. “Direct precollecting lymph vessel” arises from the lymph capillary plexus in the dermis or galea layer and directly links the collecting lymph vessels in the subcutaneous tissue (Figs. 1.2, 1.3 and 2.89). “Indirect precollecting lymph vessel (or bridge precollecting lymph vessel)” arises from the lymph capillary plexus in the dermis and crosses the subcutaneous tissue, bypasses collecting vessels to reach the galea layer where it merges with the other precollecting lymph vessels and then travels to the subcutaneous tissue again to link the collecting lymph vessels, which explains the lymphatic drainage between the dermis and the galea layer in the scalp (Figs. 1.2 and 2.89).
4.1 Direct Precollecting Lymph Vessels (Figs. 1.2, 1.3, 2.2, 2.3, 2.9 and 2.10, 2.50, 2.51, 2.52, 2.53, 2.54, 2.55, 2.56, 2.57, 2.58, 2.59, 2.60 and 2.65, 2.68, 2.69, 2.70, 2.71, 2.72, 2.73, 2.74, 2.75, 2.76, 2.77, 2.78, 2.79, 2.80, 2.81, 2.82, 2.83, 2.84, 2.85, 2.86, 2.87 and 2.88)
4.1.1 Head and Neck
