Table Of ContentJudit Daroczy
The Dermal
Lymphatic Capillaries
With 174 Figures
Springer-Verlag
Berlin Heidelberg New York London Paris Tokyo
Dr. Judit Daroczy
Kallai Eva Hospital
of State's Hospital Stephan
Kun n.4
1081 Budapest, Hungary
Library of Congress Cataloging-in-Publication Data
Daroczy, Judit. The dennallymphatic capillaries. Bibliography: p. Includes index.!. Skin - Lymphatics -
Ultrastructure. I. Title. [DNLM: 1. Lymphatic System. WH 700 D224d] QM197.D37 1988 611'.4288-22421
ISBN-13: 978-3-642-73482-3 e-ISBN-13 978-3-642-73480-9
DOl 10.1007/978-3-642-73480-9
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Preface
The importance of the lymphatic system has been known for a long time. It was
therefore surprising to learn that the status of dermal lymphatics, under both
normal and pathological conditions of man, had been largely neglected to date,
particularly with respect to their ultrastructure. Moreover, the existing informa
tion is incomplete, relating only to narrow segments of the skin, and it is con
troversial.
This monograph represents an effort to overcome some of the existing defi
ciencies in the area of the structure (with emphasis on ultrastructure) of lym
phatic capillaries. It is an account of our experience in the evaluation of dermal
lymphatics in normal, edematous, and some other pathological conditions in
man and in experimental animals.
It is hoped that this information will prove useful for other investigators as a
basis for evaluation of the structural and functional status of dermal lymphatics
under a wide variety of pathological conditions. To the best of my knowledge,
much of the information on the ultrastructure of the dermal lymphatics pre
sented herein is new.
This work would not have been possible without the inspiration of Prof. Dr.
I.ANTON-LAMPRECHT, Head of the Institute for Ultrastructure Research of the
Skin, Department of Dermatology of the University of Heidelberg, Federal
Republic of Germany.
I gratefully acknowledge the generous support of the Alexander von Hum
boldt Foundation of Germany, which enabled me to carry out a major portion
of the work upon which the monograph was based, in Heidelberg.
Budapest, August 1988 Dr. JUOIT DAROCZY
Table of Contents
Materials and Methods
1 The Lymphatic Tree . 2
1.1 Lymphatic Trunk 2
1.2 Lymphatic Collecting Vessels 2
1.3 Lymphatic Capillaries. . . . . 2
2 How to Demonstrate Lymphatic Capillaries . 4
3 How to Identify Lymphatic Capillaries ... 5
4 Morphological Features of the Dermal Lymphatic Capillary 18
4.1 Pericapillary Connective Tissue ....... . 18
4.1.1 Basal Lamina ............. . 18
4.1.2 Endothelial Cytoplasmic Pseudopodia 18
4.1.3 Connective Tissue Microfilaments ... 18
4.1.4 Attachment Plates Along the Capillary Wall 19
4.1.5 Elastic Fibers . 19
4.1.6 Collagen Fibers ...... . 20
4.2 Endothelial Cells ......... . 20
4.2.1 Cytoplasmic Microfilaments 20
4.2.2 Microtubules ..... 20
4.2.3 Multivesicular Bodies. 21
4.2.4 Golgi Apparatus 21
4.2.5 Centrioles ...... . 21
4.2.6 Mitochondria .... . 21
4.2.7 Endoplasmic Reticulum 21
4.2.8 Ribosomes .. . 21
4.2.9 Cilia ..... . 21
4.2.10 Lipid Droplets . 21
4.2.11 Vesicles ... . 21
4.2.12 Lysosomes .. . 22
4.2.13 Dense Granules 22
4.2.14 Tubuloreticular and Crystalloid Inclusions 22
4.2.15 Nucleus 22
4.3 Innervation ...... . 22
5 The Lymphatic Valve System 46
5.1 Structure of the Valves . 46
5.1.1 Connective Tissue 46
5.1.2 Basal Lamina . . 46
5.1.3 Endothelial Cells . 46
VIII Table of Contents
5.2 Main Forms of the Lymphatic Valves 47
5.2.1 Joining Valves . . . 47
5.2.2 Segment Valves . . 47
5.2.3 Unicellular Valves. 48
5.2.4 Bunch Valves 48
5.3 Inlet Valves . . . . . . . . 49
6 Lymphaticovenous Anastomoses 76
7 Lymph Formation and Lymph Flow 77
8 Function of the Dermal Lymphatic Capillaries 80
8.1 Functional Morphology 80
8.2 Manner of Function ............ 81
9 The Role of Interstitial Proteolysis and Macrophages . 84
10 Pharmacology of the Dermal Lymphatic Capillaries 85
11 Inflammatory Conditions . . . . . . . . . . . . . . . 87
11.1 Morphological Changes
of the Dermal Lymphatic Capillaries During Inflammation 87
11.2 Regeneration of the Lymphatic Capillaries . 87
11.3 Cellular Components in the Capillary Lumen
and in the Pericapillary Space. . . . . . . . . 87
11.4 Role of the Lymphatic Capillaries in the Development
of Cellularlmmunity . . . . . . . . . . . . . . . . . . 89
12 Mechanism of Transport Through the Lymphatic Capillary Wall 100
13 Insufficiency of Lymph Flow . . . . . . . . . . . . . . . . 101
13.1 Safety-Valve Function of Lymph Flow. . . . . . . . 101
13.2 Dynamic Insufficiency (High Lymph-Flow Failure) . 101
13.3 Mechanical Insufficiency (Low Lymph-Flow Failure) . 101
13.4 Safety-Valve Insufficiency. 101
14 Forms of Lymphedema . . . . . 102
14.1 Classification of Lymphostatic Edema 102
14.2 Clinical and Morphological Stages of Lymphostatic Edema 102
14.2.1 Latent Edema . . . . . . . . . 102
14.2.2 Manifest Edema (Reversible) . 103
14.2.3 Manifest Edema (Irreversible) 103
14.2.4 Elephantiasis. . . . . . . . 103
14.3 Inflammatory Skin Conditions
Leading to Chronic Lymphedema 103
14.3.1 Usual Forms. . . . . . . . 103
14.3.2 Rare Forms ....... . 104
14.4 Diagnosis of Lymphostatic Edema 104
14.5 Histological and Electron-Microscopical Features
of Lymphostatic Edema . . . . . . . . . . . . . . . 105
Table of Contents IX
15 Tumors of the Dermal Lymphatics 122
15.1 Lymphangioma . 122
15.1.1 Congenital ..... . 122
15.1.2 Acquired ...... . 123
15.2 Lymphangiosarcoma (Stewart-Treves Syndrome) 123
15.3 Pseudo Kaposi's Sarcoma. 124
15.4 Kaposi's Sarcoma ... 124
16 Lymphovascular Alterations
in Different Syndromes Related to Dermatology 134
16.1 Melkersson-Rosenthal-Mischer Syndrome 134
16.2 Klippel-Trenaunay-Weber Syndrome 134
16.3 Nonne-Milroy-Meige Syndrome. 134
16.4 Noonan's Syndrome 134
16.5 Maffucci's Syndrome . 134
16.6 Yellow Nail Syndrome 134
17 Diabetes mellitus ..... . 135
18 Aged-Related Changes of Dermal Lymphatics 136
19 Lymphovascular Alterations in Selected Dermatological Diseases 137
19.1 Porphyria Cutanea Tarda . . 137
19.2 Hyalinosis Cutis et Mucosae 137
19.3 Lichen Amyloidosus . 13 7
20 Lymphangitis ........................ 144
20.1 Lymphostatic Lymphangitis and Edema . . . . . . . 144
20.2 Sclerosing Non-venereal Lymphangitis of the Penis. 144
20.3 Syphilis . . . . . . . . . . . . . . 144
20.4 Parasitic Lymphangitis ..... 144
20.5 Lymphangitis in Mucormycosis. 145
20.6 Lymphangitis due to Irritants. 145
20.7 Lymphangitis Carcinomatosa . 145
21 Treatment of Lymphostatic Edema . 148
21.1 Drug Therapy . . 148
21.2 Physical Therapy 148
21.3 Surgial Therapy 149
References . . 150
Subject Index 155
Materials and Methods
Human Material. Normal and pathological skin Cleveland, Ohio) 20 min before being killed.
of the forearm, lower leg, and back were stud Tissue samples from the upper and lower paws
ied. The biopsies were taken from the follow were taken from the animals under ether
ing disorders (under local anaesthesia): anesthesia. Blocks of skin from the upper and
lymphedema, hyperkeratosis, atrophic skin le lower paws were fixed in KARNOVSKY'S fixative
sions, ichthyosis vulgaris, pityriasis rubra pila (KARNOVSKY 1965) and postfixed in OS04 with
ris, toxicoderma, lymphangioma circumscrip lanthanum according to SHEA (1971). The par
tum, pseudo-Kaposi's sarcoma, Kaposi's sarco affin embedded materials were stained with he
ma, porphyria cutanea tarda, hyalinosis cutis et matoxylin and eosin, orcein, GOMORI'S silver
mucosae, lichen amyloidosus, lymphangitis impregnation, and WEIGERT'S resorcin-fuchsin
carcinomatosa. staining. The samples for electron microscopic
Experimental Material. Canine: Male and studies were fixed by immersion using KAR
female canines weighing 15-25 kg were used NOVSKY'S fixative and postfixed with OS04
for this study. Lymphedema was produced by (DAROCZY and HUTTNER 1978). The tissues
the ligation of the lymphatic trunk in the femo were treated for 2 h with uranyl acetate en bloc
ral region (SOLTI 1986). Skin biopsies were tak and embedded in Epon. The semithin, tolui
en from the normal hind limbs and from the dine-blue stained sections were reviewed by
operated extremities of the animals after light microscopy. The thin sections were cut
10-14 days they were operated. Rat: Wistar with Reichert Vm02 ultrotome and examined
rats weighing 150-200 g were injected i. v. with either unstained or following uranyl acetate
50 gl100 g body weight of native ferritin (dia and lead citrate staining with JEM 7A and
lysed, Nutritional Biochemicals Corporation, Philips EM-600 microscopes.
2
1 The Lymphatic Tree
The phylogenesis and comparative anatomy is prominent along the wall segments between
are described for the large lymphatic vessels the valves. The elastic fibers do not form an
and trunks (TONDGRY and KLBIK 1972). The elastic membrane, but rather a loose network
lymphatic tree (human) can be grouped into accompanied by fibroblasts in the tunica ad
three categories. ventitia (OEHMKE 1968; LEAK 1972 a). Unmyel
inated nerve bundles can be present. The col
lecting lymphatic vessels contain valves and
1.1 Lymphatic Trunk they have a well-developed basal lamina. The
endothelial junctions are tightly closed; thus,
large molecules and cells can not escape from
The lymphatic trunk represents the thoracic
the vessels but water and small molecules may
duct and empties into the great veins of the
migrate outward.
neck. The vessel contains valves and the wall
consists of three distinct tunics: (a) the tunica
mtIma, compnsmg endothelial layer sur
rounded by basal lamina, (b) the tunica media, 1.3 Lymphatic Capillaries
consisting of alternating layers of smooth mus
cle cells and collagen and elastic fibers, and (c)
The smallest lymphatic vessels have been
the tunica adventitia, composed of collagen
termed "terminal lymphatics", "smalllymphat
and elastic fibers intermingled with fibroblasts,
ics", or "initial lymphatics". The different ter
in addition to nerve bundles and small blood
minologies are misleading; like the small blood
vessels.
vessels they are classified as capillaries. They
contain valves, and the permeable wall consists
of endothelial cells. The presence of endotheli
1.2 Lymphatic Collecting Vessels
al gaps is common, and a continuous basal
lamina is lacking. In the perivascular intersti
The lymphatic capillaries empty into the lym tium the elastic fibers are intermingled with
phatic collecting vessels. The collecting vessels collagen fibers and with the micro filaments
are punctured with lymph nodes. They lie in running directly to the abluminal membrane of
the mid and deep dermis, especially at the junc the capillary endothelial cells.
tion of the dermis with the subcutaneous tissue The lymphatic plexus begins in the dermis
and in the septa of fat lobules. The form of as blind tubes in the dermal papillae; these join
their luminal cross sections depends on the with neighboring capillaries to form the super
phase of their activity. The vessels can be oval, ficial lymphatic plexus. The deep lymphatic
round, cruciform, or star-shaped. plexus is composed of lymphatics of varying
The collecting vessels have three wall lay caliber, which are situated in the deeper layers
ers: beneath the endothelial tunica intima the of the dermis (ZSDANOV 1952).
smooth muscle cells create the tunica media. PFLEGER (1964 a) described postcapillary
The muscle cells are intermingled with collagen lymphatics which were situated at the cutis
and elastic fibers. At the basis region of the subcutis boundary. In their wall, smooth mus
valves the smooth muscle layer is lacking, but it cle cells could be demonstrated.
Lymphatic Capillaries 3
The term ''dermal lymphatic capillary" repre (eASLEy-SMITH and SIMS 1976). The lymphatic
sents a lymph vessel lacking continuous basal lumen contains flocculent material which ap
lamina and smooth muscle cells in its wall. pears medium dense under the electron micro
The term "prelymphatics" represents the scope and it is interpreted as being protein-rich
path of least resistance through the connective lymph. This flocculent material is observed in
tissue directed toward the lymphatics. They are the adjacent perilymphatic areas as well.
preformed paths in the vicinity of lymphatics