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The Mammalian Carotid Body PDF

98 Pages·1987·3.739 MB·English
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Advances in Anatomy Embryology and Cell Biology Vol. 102 Editors F. Beck, Leicester W Hild, Galveston W Kriz, Heidelberg R. Ortmann, KOln J.E. Pauly, Little Rock T.H. Schiebler, Wiirzburg David J. Pallot The Mammalian Carotid Body With 35 Figures Springer-Verlag Berlin Heidelberg New York London Paris Tokyo David John Pallot, B.Sc., Ph.D. Department of Anatomy, Medical Sciences Building, University of Leicester, Umversity Road, . Leicester LEt 7RH, Great Britain ISBN-13: 978-3-540-17480-6 e-ISBN-13978-3-642-71857-1 DOl: 978-3-642-71857-1 Library of Congress Cataloging-in-Publication Data Pallot, D.J. (David J.) The mammalian carotid body. (Advances in anatomy, embryology, and cell biology; vol. 102) Bibliography: p. Includes index. 1. Carotid body. 2. Mammels-Physiology. I. Title. II. Series: Advances in anatomy, embryology, and cell biology; v. 102. [DNLM: 1. Carotid Body. WI AD433K v. 102fWL 102.9 P168m] QL801.E67 vol. 102 574.4 s 87-4290 [QP368.8] [599'.0142] This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in other ways, and storage in data banks. Duplication of this publication or parts thereof is only permitted under the provisions of the German Copyright Law of September 9, 1965, in its version of June 24, 1985, and a copyright fee must always be paid. Violations fall under the prosecution act of the German Copyright Law. © Springer-Verlag Berlin Heidelberg 1987 The use of general descriptive names, trade names, trade marks, etc. in this publication, even if the former are not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone. Product Liability: The publisher can give no guarantee for information about drug dosage and application thereof contained in this book. In every individual case the respective user must check its accuracy bv consuitinJ!; other phaimaceutica1 literature. Contents 1 Introduction 1 2 Ultrastructure of the Carotid Body 10 2.1 Type I Cells 11 2.2 Sub-types of Type I Cells 15 2.3 Type II Cells 20 2.4 Ganglion Cells 21 2.5 Blood Vessels 22 3 Innervation of the Carotid Body 25 3.1 Ultrastructure of Nerve Endings 25 3.2 Clear-Cored Vesicles 26 3.3 Mitochondria 29 3.4 Electron Dense-Cored Vesicles 29 3.5 Glycogen Granules . 29 3.6 Varieties of Type I Cell Endings 31 4 Catecholamines and the Carotid Body 38 4.1 Effects of Natural Stimuli on Carotid Body Catecholamines 41 4.2 Synthesis of Catecholamines . 43 4.3 Uptake and Metabolism of Catecholamines 44 4.4 Effects of Catecholamines on Carotid Body Activity 44 4.5 Sites of Action of Catecholamines 46 5 Carotid Body Pathology . 50 5.1 The Human Carotid Body and Chronic Hypoxaemia 50 5.2 Chronic Hypoxaemia in Animals . 53 5.3 Carotid Body Hyperplasia in Systemic Hypertension 59 5.4 Chemodectomas 63 5.5 The Carotid Body and Cot Death 65 6 Identity of the Chemosensor 69 6.1 The Type I Cell 69 6.2 Studies of Neuromas 72 7 Conclusion 76 Acknowledgments .. 77 References . 78 Snbject Index 90 VI 1 Introduction According to Valentin (1833) and Luschka (1862), the first description of the structure now known as the carotid body must be ascribed to a Swiss physiolo gist - Albrecht von Haller - who, in 1762, called it the ganglion exiguum. This claim, however, may be erroneous, for Tauber (1743) described a struc ture at the bifurcation on the common carotid artery and called it the ganglion minutum. Andersch (1797) reprinted the text of a study made by his father between 1751 and 1755. The original printing of this work had apparently been sold as waste paper! Andersch called the organ the ganglion intercaroticum on account of its location. He also specifically stated that the sympathetic chain, the glossopharyngeal and the vagus nerves sent branches into the organ. For a while the carotid body remained forgotten, to be rediscovered in 1833 by Mayer of Bonn who again remarked upon the branches of the sympathetic, glossopharyngeal and vagus nerves as sources of a nerve plexus which innervated the ganglion intercaroticurtl.. Valentin (1833) clearly regarded the structure as part of the sympathetic nervous system, although he too recognised that the vagus and glossopharyngeal nerves contributed conspicuously to its innervation. Thus it is evident that the anatomists of the eighteenth and early nineteenth centuries regarded the structure in the carotid bifurcation as one of the many ganglia which are interspersed in the course of the sympathetic nervous system. The carotid body received little attention for the next 30 years, until micro scopical investigation became more fashionable. Beginning with the work of Luschka (1862), the search for its microscopical nature touched off a controversy which has lasted until recent years. Luschka's studies revealed that the organ was not a ganglion but a glandular structure, rich in nerves and blood vessels; thinking it was derived from endoderm, he named it the glandula carotica. Hence he was the first to break with the tradition of interpreting the structure as that of another sympathetic ganglion. He was undoubtedly also the first to recognise the glandular character of the organ and, by recognising its morpho logical similarity to the adrenal and pituitary glands, of started the line of thought which holds that the carotid body m"ay have an endocrine function. Arnold (1865) rejected Luschka's interpretation and insisted that the structure was no more than a vascular glomerulus; he named it glomeruli arteriosi intercar otica and considered that the chief cells in it were derived from endothelial cells of the blood vessels. At about this time the field of embryology was gaining increasing importance. Stieda (1881) observed a thickening of the epithelium of the third branchial arch and regarded it as the anlage of the carotid body, since this proliferation was close to the carotid bifurcation. Kochenko (1887) declared that the carotid body was not a derivative of the branchial arches but developed from a proliferation of the wall of the internal carotid artery. 1 Subsequently, the glossopharyngeal nerve, vagus nerve and cervical sympathetic trunk made contact with the organ. Similar nervous contacts were described by Marchand (1891), Paultauf (1892) and Verdun (1898). However, these studies did little to help in comprehending the function of the organ, and the question still remained as to whether it should be classified as a mere vascular glomerulus, a gland, part of the autonomic nervous system or a combination of these possibilities. Stilling (1898) first described a chromaf fin reaction. in the carotid body. Since Henle (1865) this reaction had been known in the adrenal medulla and was thought to be a specific technique for the histochemical detection of adrenaline and other amine-like substances. The chromaffinity, or otherwise, of carotid body cells has since been one of the most disputed questions in the anatomical study of the chemoreceptors. In 1903 Kohn defmed the carotid body as being derived from neuroectoderm, innervated by preganglionic sympathetic nerve fibres and showing a positive chromaffm reaction; he considered the organ to be similar to the adrenal me dulla and other paraganglia and hence used the term paraganglion intercaroti cum. Kose (1907), one of the protagonists of Kohn's paraganglion theory, did not see a chromaffin reaction in all the carotid body cells and therefore called them Farblose Chromaffin Zellen - clear chromaffin cells. The work of Gomez (1908) established that the carotid body contained two specific cell types, which we will refer to as Type I cells and Type II cells (see below). The carotid body again went into obscurity for the next 20 or so years, receiving only occasional mentions in textbooks of histology under headings such as 'Endocrines', 'Chromaffin Tissue' and 'Paraganglion Caroticum' and, in one or two English texts, under the non-committal term 'carotid body'. The most outstanding contribution to the knowledge of the significance of the carotid body was made by Fernando de Castro of Madrid in the latter half of the 1920s. Between 1926 and 1928 he performed the first systematic studies of the innervation of the carotid body, using methylene blue and silver techniques. He noted numerous nerve fibres and terminals in association with the parenchymal cells, and described the following essential features of carotid body nerve fibres (de Castro 1926, 1928; also see Eyzaguirre and Gallego 1975): 1. Individual nerve fibres undergo branching to innervate many cells often lo cated in different glomeruli. 2. Cells may be innervated by more than one nerve fibre. 3. A single nerve fibre may give rise to terminals displaying variable morpholo gies, including small boutons, cup-shaped (calyceal) endings and large plate like endings; nerve terminals often give rise to fibres forming terminals con tacting other cells. 4. Nerve fibres and terminals in the carotid body are derived primarily from the carotid sinus nerve (a branch of the glossopharyngeal nerve), section of which produces degeneration of fibres and terminals within the carotid body. De Castro (1928) sectioned the rootlets of the glossopharyngeal nerve intra cranially and examined the carotid bodies 12 days after this surgery. He observed no degenerative changes and concluded that the nerve endings on the cells were sensory, with their cell bodies located in the ganglion of the glossopharyn geal nerve. It was further postulated that the principal cells of the carotid body, 2 were chemoreceptors and that their sensory innervation was through the carotid sinus (Hering's) nerve which de Castro called intercarotidien because Hering's nomenclature defmed neither the anatomical distribution (both to sinus and glomus) nor the function of the nerve (pressoreceptor and chemoreceptor) path ways. These morphological studies by de Castro firmly established the existence of two types of sensory receptor at the level of the bifurcation of the common carotid artery - those associated with the carotid sinus and those associated with the carotid body. De Castro proposed that the carotid body was not a paraganglion but a chemoreceptor; this latter idea was based on his histologi cal observations that the chief cells appeared to have one pole located adjacent to a blood vessel (pole sanguin) and the opposite pole associated with nerve endings (pOle nerveux). During the same period, C. and J.F. Heymans were studying the physiology of the area of the carotid bifurcation and provided evidence that this area was a peripheral reflexogenic area sensitive to hypoxia, hypercapnia and blood pressure change (Heymans and Heymans 1927; Heymans et al. 1933). Record ings of activity from the whole carotid sinus nerve, which revealed increased neural discharge in response to asphyxia (Heymans and Rijlant 1933), confirmed the belief that a structure innervated by this nerve was a sensory organ that responded to changes in blood chemistry, and hence supported the theories of de Castro. During the 1930s, when the chemoreceptor theory of de Castro was becom ing popular, Kohn's paraganglion theory was essentially revised by Watzka (1931, 1938, 1943) and Penitschka (1931). They classified the paraganglia ac cording to two categories - chromaffin paraganglia originating from the sympa thetic nervous system and non-chromaffin paraganglia derived from the para sympathetic nervous system. According to these authors, the carotid body was representative of the non-chromaffin paraganglia. During the 1950s and 1960s the fluorescent methods for the histochemical demonstration of biogenic monoamines appeared. Eranko's method (1952) of detecting amine-storing cells was applied to the study of the carotid body by Muscholl et al. (1960), Rahn (1961), Niemi and Ojala (1964) and Palkama (1965) in a variety of species. All authors found that some cells of the carotid body showed fluorescence after fixation with formalin. The improvements in amine location brought about by the introduction of freeze-drying and formaldehyde gas treatment by Falk and Hillarp in the 1960s enabled a far better localisation of biogenic amines than did the previous methods. Numerous studies of the carotid body with this new sensitive histochemical technique established that the majority of carotid body chief cells, in a variety of species, showed distinct formaldehyde-induced fluorescence; hence it was concluded that the carotid body must contain biogenic amines (see Biscoe 1971 for review). The early work on the embryological derivation of the carotid body sug gested three possible sources for its cells: (a) neuroblasts migrating down the cranial nerves; (b) sympathoblasts from the superior cervical ganglion; and (c) mesenchymal cells from a primary condensation on the third branchial arch. The early work of many authors utilised the chromaffin reaction. Some of these authors considered the carotid body as a derivative of the sympathetic nervous system because it showed some positive chromaffin reaction; the nega tive chromaffin reaction of many cells, on the other hand, led others to believe 3 that the cells from which the developing carotid body is composed were mesen chymal in origin. Using fluorescent techniques, Korkala and Hervonen (1973) showed that in the 7-week human fetus three types of cells were observed in the environs of the carotid body. The primordium consisted of non-fluorescent fibroblasts and weakly fluorescent small cells with rounded nuclei. Similar cells were found in the sympathetic anlage and also in a cord of cells connecting the two struc tures. Amoqg these two types of cells a third, moderately fluorescent, cell type was also seen. In the 9-week fetus the fluorescent intensity of the carotid body cells increased and the connecting cord of cells disappeared; at 11-16 weeks the carotid body was a separate entity with non-cellular contacts to the sympa thetic trunk. These studies suggested that the mammalian carotid body might have a dual origin - a neural one which gives rise to the Type I cells and perhaps to some of the Type II cells, and a mesenchymal one which gives rise to the remaining cells, fibroblasts, etc. Such a view would be in keeping with the immunocytochemical studies of Abramovici and Pallot (1986), for Type I cells are rich in neuronal specific enolase, while Type II cells stain with antibodies to glial fibrillary acidic protein. The only animal in which the origin of the carotid body is established is the bird. By the formation of chimaeras from quail and chicken embryos, in which the two cell lines are easily distinguished on the basis of nucleolar mor phology, Le Douarin et al. (1972) demonstrated that the Type I cells and possi bly the Type II cells were derived from the neural crest. The carotid body in the majority of mammals is located somewhere near the bifurcation of the common carotid artery (Fig. 1) and may be associated with any of the arteries arising from the general area of the carotid bifurcation - internal carotid, external carotid, occipital or ascending pharyngeal-depend ing upon species (de Kock 1959, 1960; Lever et al. 1959; Ross 1959; Biscoe 1971). In amphibians the carotid labyrinth, a swelling at the termination of each common carotid artery, is regarded as the homologue of the carotid body (Adams 1958; Kobayashi 1971a, b; Rogers 1963). In birds the carotid body is found lateral to the common carotid artery in close proximity to the ultimo branchial body (de Kock 1958; Kobayashi 1971) and is sometimes completely surrounded by parathyroid tissue forming a parathyroid/carotid body complex (Kobayashi 1969, 1971 a). The mammalian carotid body is invested with a collagenous capsule which varies in thickness, depending upon the species studied. In light microscope sections the carotid body is seen to consist of groups of cells situated in a highly vascular connective tissue stroma, the individual cell groups being sepa rated by variable amounts of connective tissue. The amount of connective tissue is species-variable and is also apparently dependent upon the age of the animal (McDonald 1981; Fig. 2). Since the amount of connective tissue varies, some species possess a compact, discrete carotid body (e.g. cat and rat), whilst in other species (e.g. rabbit and adult sheep) the organ is rather diffuse. Even at the light microscope level, two different cell types can be distinguished on the basis of nuclear staining pattern and morphology (Gomez 1908). One cell type possesses a strongly basophilic nucleus and is rather elongated in shape, whilst the other is more spherical and has a less basophilic nucleus. These two cell types have received various names (see Biscoe 1971); the terms Type 4 • a Fig. 1.-c. Diagrammatic representation of the location of the carotid body (not to scale) in (a) the cat, (b) the rat (redrawn from McDonald 1981) and (c) the cow (drawn from Arias Stella and Bustos 1976). In (a) the dual innervation of the carotid body is illustrated. Note that in the cow, Arias Stella and Bustos found the carotid body in a number of different locations. ap, ascending pharyngeal artery; eb, carotid body; ee, common carotid artery; es, carotid sinus; ee, external carotid artery; em, external maxillary artery; ggn, ganglioglomerular nerve; ie, internal carotid artery; ng, nodose ganglion; 0, occipital artery; os, occipital sinus; seg, superior cervical ganglion; sin, superior la- ryngeal nerve; sn, sinus nerve; X, vagus nerve c I cells and Type II cells will be used here as they imply no functional characteris tics or properties. The Type I cells are arranged in small spherical or cylindrical anastomosing cords and are enmeshed in a skein of interlacing nerve fibres and fine capillary branches (Fig. 2). They are ovoid or polygonal in shape, with a large round nucleus, and are often separated from the capillary wall by processes of the second variety of cell, the Type II cell. In addition, the Type II cells partially surround groups of Type I cells. In routine histological sections, the most outstanding feature of all carotid bodies is the immense vasculature (Figs. 2-4). Within the organ there are arte rioles, capillaries (often incorrectly referred to as sinusoids) and small veins. Ballard et al. (1981), estimated that some 25% of total volume is occupied by these vessels in the cat carotid body (see below). In the pages that follow, we will review the ultrastructural features of the carotid body in more detail and then discuss some functional aspects of the 5

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