The Anatomy Qf Lymph Vessels in Relation to Function
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54 Lymphology 10 (1977) 54-61 © Georg Thieme Verlag Stuttgart The Anatomy Qf Lymph Vessels in Relation to Function F. Huth, D. Bernhardt Pathologic Institute, University of Dlisseldorf (Chairman: Prof. Dr. H. Meessen) The essential functions of the lymphatic sys -Natucci and Zaccharini 1949; Rusznyak, tem are to pi~k up large molecules, particles Foldi and Szabo 1957; Hankiss 1959; Aiello and excess fluid and to transport them from et al. 1960; Tormene et al. 1965; Csillik and the peripheral connective tissue to the venous Foldi 1967; Huth et al. 1970; Foldi 1971; system. Within normal tissue most of the Stroobandt et al. 1976; Lie et al 1976; lymphatics are collapsed, (Fig. la). They can, Huth et al. 1974, 1976). Oemer et a1. (1972) therefore, hardly be differentiated light micro modified the method of blocking the lymph scopically from blood capillaries or from outflow by interrupting the thoracic duct. septal connective tissue. Various techniques The possibility of huge dilation of the lym have been used to visualize the lymph vessels phatics is different from the limited dilatation within organs and extremities. Retrograde in rate of the blood capillaries (Fig. 2a). Electron jection of air, indian ink, differ~nt proteins microscopy demonstrates that additional and dyes, silver nitrate, mercur}r, ferritin, properties of lymph· capillaries exist in con acrylic resins etc., often lead td ruptures of trast to blood capillaries ( Casley-8mith 1965, the thinwalled and vulnerable lYmphatics, 1967, 1910;Burke and Leak 1965, 1970; there by causing interstitial dye bxtravasates Huth 1967, 1968; Huth et al. 1970). The to be falsely interpreted as lymphatics ( Wutzer thickness of the lymphatic endothelium can 1834, Most 1908, Bartels 19091 Baum 1928, vary from 0.1 /l to several micra. In contrast Grau 1943, Jancso et al. 1952,fMori 1963, to blood capillaries, the lymphatic endotheliwn Mori et al. 1964, Leak and Burke 1966t is not enveloped in a continous basal lamina Viragh et al. 1966, Bergstrom ~d Werner or pericytes (Figs. 1, 2a, b, c; d). Similar to 1966, Kuprianov 1969, Casley-Smith 1969, blood vascular endothelium, it contains mito Gerteis 1972). Injection of lyniph-specific chondria, lysosomes, free ribosomes, a scant dyes such as patent blue as weti as different endoplasmic reticulum, fine intracytoplasmic tracer techniques demonstrate ~ectorallymph I muscular fllarnents, and sometimes numerous vascular branches but never the complete microvesicles. The endothelial processes link lymph drainage of tissue or organs. Application to each other multiformally: Apposed of hydrogen peroxide demonst~tes the l~ph membranes can be held together by maculae vessels below mesothelial surfaces; total occludentes or adherentes (Fig. 3b). Some lymphangiography of an orgart was not pos times the cellular margins are connected by sible with this method (Magnus i922, 1923, interdigitations (Fig. 3a); in other areas, a Hass 1936, Johnson and Blak~ 1966; John- 1 close apposition without special cellular pro son 1969). 1 trusions dominates. A specific structure of In 1939 Kaiserling and Soostrizeyer found a lymph capillaries is represented by the over way out of this methodologicil problem by lap of endothelial cell processes. The gaps be blocking the lymph flow of w?- organ like the. tween the overlapping cell processes can separate up to several micra so that complete kidney. This procedure leads ~o a lymphostasts with dilatation of the lymph vascular branches cells from the interstitium can readily pass (Fig. 1b) up to their capillary endings which the patent junction (Fig. 2b). The ~atency ~of thus can be seen light microsCopically. Other the junctions is influenced by another specific investigators used this method with success in structure: Leak and Burke (1968) were able· various organs (Romualdi et al. 1946, 1947; to demonstrate fme anchoring ftlaments Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY. The Anatomy of Lymph Vessels in Relation to Function 55 emanating from the outer surface of the lymphatic endothelium and extending into the interstitium with its thicker collagen fibrils (Fig. 3b). The overlap of endothelial cells with the possibility of extensive patency and the anchoring fllaments maintain the removal of interstitial fluids and corpuscular substances and/or large molecules. Increased interstitial hydrostatic pressure will expand the interstitial space, hereby drawing the collagen fibrils. In this way the intercellular clefts are opened by pulling the :filaments attached to the endothelial wall. This adap tive mechanism of lymphatics in response to altered hydrostatic and osmotic interstitial pressure has been proven not only in sub cutaneous connective tissue (Casley-Smith 1967, Leak 1972) but also in other organs such as the kidney, the liver, and the heart (Huth 1968; Huth·et a!. 1970, 1976; Lie et al. 1976; Stroobandt et al. 19176). Kalima and Kalima (1975) demonstrated different gaps between the overlapping endothelial processes of mesenteric lymphatics. They referred to them as perilymphatic channels. They thought the channels played a signifi cant role in the uptake of liquids or sub stances into the lymphatics. We saw compar able structures in organ lymphatics (Fig. 2d). Casley-Smith used the term prelymphatic for all interstitial spaces which are finally drain- ed by lymphatic vessels. The trel)1endous dilatation rate of the lymphatics caiu1ot be Fig la Nearly collapsed lymph capillary of the heart musCle. x 19.120 completely explained by the special connections. 1 b Dilated lymph collecting vessel with valves with of the endothelial cellular processes. A further in the renal hilus, following experimental lympho extending capacity such as an intensive fold stasis of the kidney. ing of the lymphatic endothelium within non 22 x, v. Giesen altered organs or tissues exists (Fig. 2f). In addition, the numerous cellular protrusions of lymphatic endothelial cells (Fig. 1a) must overlapping cell processes together thus clos be regarded as a structural reserve for dilation ing the junctions. At this point one could since they disappear during dilation. It was speculate that the peripheral lymph drainage Casley-Smith (1967), Foldi (1972), and Leak system functions adequately until the endo (1972) who differentiated between L'1e spe thelial junctions are pulled too far apart and cial manner of transpoting fluids, proteins, lymph fluid can again escape. and lipids via draining iymph vessels and the Uptake of particles and fluids into lymphatics characteristic submicroscopical structures. from the interstitium can also occur across Increased interstitial pressure leads to opening the endothelium within multiple vesicles of the endothelial junctions while higher pres (Fig. 3b). The transcellular passage has been sure inside the vascular lumen presses the elucidated by experiments with different parti- Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY. 56 F. Huth, D. Bernhardt Fig. 2a Dilated lymph capillary between blood capillaries of myocardium. x 3. 75 0 2 b Open junction between two endothelial processes of a lymph capillary. x 13.800 2c Dilated lymph capillaries with endothelial siderosomes, following venous congestion. x 4 000 2d Dilated lymph capillary with splitting of an endothelial cell, forming a perilymphatic channel (above). X 3.675 2e "Confluence" of several lymphatics at the inner surface of the chylous cisterna. x 230 2f Top view of lymph vascular endothelium with intensive folding of the endothelial cells. x 600 Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY. The Anatomy of Lymph Vessels in Relation to Function 57 b c Fig. 3a Interdigitation of two endothelial processes in the lymph capillary wall. x 29.500 3b Part ly transversa lly, partly ta ngentially sectioned lymph capillary with intensive microvesiculation of the endothelium beside the adjacent co llagen fibrils and finer filaments. Zonula occludens formed by two endothelial cell processes at the right below. 44.250 x 3c Parasitic Iymphangiosis (onchocercosis). HE, 60 x cles and substances (Casley-Smich 1964, 1965, scopy and scanning electron microscopy, it 1968; Leak and Burke 1966, 1968). The has been proven that funnel-like valvular further transport of lymph following its re structures dominate (Lauweryns 1971 ). Blood sorption is maintained by valves which can vessels, i.e. veins of comparable size, do not alieady be observed in smaller lytnph-collecting contain valves. The existence of valves, there vessels like those of the epicardium or the fore, support the identification of medium hilar lymph vessels of different organs sized lymph vessels. Within the lymph-col (Fig. 1b ). Lymph vascular valves differ in lecting vessels, not only the valves but also a size and shape. With the aid of stereomicro- special wall structure helps to propel the Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY. 58 F. Huth, D. Bernhardt lymp~ centripetally. Lymph propulSion by valves in cases without carditis have been cor rythmic contractions has been dembnstrated related with lymphostatic conditions (Kline experimentally in vivo and in vitro ~y Florey 1964, Miller et al. 1960-70, Goldberg 1968, (1927), Smith (1949), Horstmann ~1951, Bullon