Intrapulmonary Airway Morphology in Three Species of Monkeys : A Correlated Scanning and Transmission Electron Microscopic Study W. L. CASTLEMAN, D. L. DUNGWORTH AND W. S. TYLER California Primate Research Center and Departments o f Veterinarg Pathology and Anatomy, University of Calfornia, Davis, California 9561 6

ABSTRACT Intrapulmonary airways were studied in rhesus (Macaca m u latta), stumptail (Macaca arctoides), and bonnet (Macaca radiata) monkeys by correlated scanning and transmission electron microscopy. Lobar, segmental, and subsegmental bronchi in all three macaques were lined by pseudostratified columnar epithelium composed primarily of ciliated cells, mucous cells, and basal cells. Neuronal processes and cells containing dense-core vesicles were also observed. Terminal bronchioles in rhesus and stumptail monkeys were short and only developed to a single generation. Terminal bronchioles were moderately longer in bonnet monkeys and were occasionally developed to two generations. Terminal bronchioles in bonnet and stumptail monkeys were lined by ciliated pseudostratified columnar epithelium which included nonciliated bronchiolar epithelial (Clara) cells. The arrangement of epithelium in terminal bronchioles differed slightly in rhesus monkeys. All three species had long respiratory bronchioles. They were lined by simple, nonciliated cuboidal and squamous epithelium which usually did not contain secretory droplets. Capillaries were often observed immediately below the luminal epithelium. Cuboidal cells containing dense-core vesicles were a rare component of the epithelium of respiratory bronchioles i n stumptail monkeys. Alveolar ducts were lined by an epithelium composed of type I and type I1 cells. The results of this study indicate that there is general similarity in the mucosal structure of bronchi and respiratory bronchioles between macaques and man but that there are differences in the number of generations and epithelial lining of terminal bronchioles.

In choosing an animal model for use in experimental studies related to human pulmonary disease processes, it is necessary to take into consideration anatomical differences and similarities which exist between the lungs of man and the various laboratory animals. McLaughlin et al. ('61) have shown that one important area of difference in pulmonary anatomy among various mammalian species is present at the level of the distal airways. Differences in distal airway morphology exist to the extent that animals such as rats and pigs have very short respiratory bronhioles, whereas animals such as cats and dogs have long, well-developed respiratory bronchioles. Experimental evidence (Gross et al., '66; Freeman et al., '73; Plopper et al., '73) indicates that distal airways, and AM. J. ANAT., 142: 107-122.

especially respiratory bronchioles, are highly vulnerable to injury from inhaled irritants. Because there is great variability in airway morphology between species and differing vulnerability of airways to pulmonary irritants, it is essential to understand how normal airway morphology in any animal compares with that of man when the animal is to be used as a model for studying the response of human lungs to inhaled irritants. A substantial amount of information is available on airway morphology in commonly used laboratory animaIs such as rats (Rhodin and Dalhamn, '56; Parkinson and Stephens, '73), mice (Karrer, '56; Greenwood and Holland, '72), hamsters (Nowell and Tyler, '71), and dogs (Frasca et al., '68; Freeman et al., '73). Little published 107

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information, however, is available on pulmonary airway morphology in nonhuman primates, even though they are being used to a n increasingly greater extent in experimental pulmonary studies. Greenwood and Holland ( ' 7 3 ) have used the scanning electron microscope to describe surface morphology in trachea, bronchi, and alveolar areas of stumptail monkeys, but no information was given on terminal bronchioles, respiratory bronchioles, alveolar ducts, or on cells below the luminal surface. The purpose of the present study was to characterize intrapulmonary airway morphology in several commonly used species of macaques and to compare it with airway morphology that has been described for man. Both scanning and transmission electron microscopy were used so that airway surface morphology could be correlated with subsurface and intracellular morphology. Airways were studied from the level of the lobar bronchus distal to alveolar ducts.

oxide, and embedding in EponIAraldite. Sections one-micron thick were cut and stained for the purpose of tissue selection. Thin sections from selected blocks were stained with lead citrate and uranyl acetate. Airways were identified as being a bronchus, terminal bronchiole, respiratory bronchiole, or alveolar duct according to criteria outlined by von Hayek ('60), Krahl ('64), and Nagaishi ('72). OBSERVATIONS

Airway types and branching patterns. Bronchi in macaque lungs were developed to at least three generations before the first bronchioles were reached. I n rhesus and stumptail monkeys, bronchi opened distally into short terminal bronchioles (average length 2-3 m m ) that were only developed to a single generation (fig, 1 ) . In rhesus monkeys, bronchi frequently opened directly into respiratory bronchioles without there being a n intermediate terminal bronchiole (fig. 2). Terminal bronchioles MATERIALS A N D METHODS were usually longer i n bonnet monkeys Lungs from three rhesus monkeys (average length 5 m m ) than i n the other (Macaca mulatta), three stumptail mon- two species and occasionally divided to keys (Macaca arctoides), and three bonnet form secondary generations. Highly alveomonkeys (Macaca radiata) were studied. larized respiratory bronchioles were obThe monkeys were killed by intravenous served in all three species of macaques (fig. injection of sodium pentobarbital, and the 3 ) and were frequently developed to seclungs were excised from the chest and in- ondary or tertiary generations. Respiratory flated via the trachea at 30 cm fixative bronchioles in all three species opened into pressure with Karnovsky's fixative (Karnov- long alveolar ducts (figs. 3, 17) which sky, '65) diIuted I : 4.5 (550 mOsm) with branched. 0.2 M cacodylate buffer. Following fixaBronchi. The mucosal structure of lotion, airways from the right cranial and bar, segmental, and subsegmental bronchi caudal lobes were bisected longitudinally. in macaques was generally similar to that The bisected halves of the airways were which has been described for man and examined under a dissecting microscope other mammalian species. The epithelial and the length of terminal bronchioles was lining was pseudostratified columnar, and measured. One half of each selected air- the predominant cell types were ciliated way was trimmed and prepared for scan- cells, mucous cells, and basal cells. Apical ning electron microscopy by dehydration portions of the mucous cells often prothrough alcohol and amyl acetate, critical jected into the bronchial lumen (fig, 4). point drying with carbon dioxide, and coat- Ciliated cells from bonnet monkeys differed ing with silver and gold. The complemen- slightly in ultrastructure from those of the tary half of each selected airway was other monkeys in that they often contained prepared for transmission electron micros- membrane-bound inclusions containing copy by dissecting the airway out from material with a fibrogranular appearance surrounding alveolar tissue, dicing it into (fig. 5). Neuronal processes not ensheathed about 1 mm? pieces, osmicating the tissue by neurilemmal cells were commonly found in Zetterqvist's osmium (Pease, '64), de- between epithelial cells, and the axons conhydrating it through alcohol and propylene tained granular and agranular vesicles.

INTRAPULMONARY AIRWAY MORPHOLOGY IN MACAQUES

The least frequently observed of all epithelial cell types in the bronchial mucosa was a granulated cell which was found at several locations in the bronchus of one rhesus monkey. These cuboidal cells were positioned against the basal lamina, beneath other epithelial cells, and contained densecore vesicles which were 95-125 n m in diameter. Terminal bronchioles. Terminal bronchioles were easily identified with the scanning electron microscope since these airways have a wall uninterrupted by alveoli and lacking cartilage and submucosal glands. Terminal bronchioles were lined by ciliated pseudostratified columnar epithelium. I n proximal bronchiolar areas, the mucosal structure was identical to that found lining bronchi. More distally, however, variations in mucosal structure were observed, and the pattern of variation differed among the individual species of macaques, In stumptail and bonnet monkeys, mucous cells became less numerous in distal bronchiolar areas and were replaced by nonciliated bronchiolar epithelial (Clara) cells. The cytoplasm of these cells contained abundant mitochondria, a medium-sized Golgi complex, and a moderate amount of granular endoplasmic reticulum. They were covered on their luminal surfaces by microvilli (fig. 6). In bonnet monkeys, the cells frequently contained round secretory droplets that were homogenously electron-dense (fig. 7). Secretory droplets were less frequently observed in the nonciliated bronchiolar cells of stumptail monkeys. At the level of the first respiratory bronchioles, there was a transition from ciliated pseudostratified columnar epithelium to nonciliated simple low columnar epithelium. This transition was usually abrupt in rhesus and bonnet monkeys (fig. 8), but was more gradual in stumptail monkeys. In rhesus monkeys, the epithelial lining of terminal bronchioles differed from that in the other two macaques. Mucous cells did not become appreciably reduced in number in distal areas of bronchioles, a s they had in bonnet and stumptail monkeys. Instead, the epithelium continued to be composed of mucous cells, ciliated cells, and basal cells down to the level of the first respiratory bronchioles where the

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transition took place between ciliated and nonciliated epithelium (fig. 8). Only past this transition point were mucous cells no longer present and did nonciliated bronchiolar epithelial cells appear. These nonciliated bronchiolar cells were not observed to contain secretory droplets. Neuronal processes were present among terminal bronchiolar epithelial cells in all three species of monkeys. Respiratory bronchioles. Initial portions of respiratory bronchioles in all species were lined continuously by nonciliated simple epithelium which was low columnar or cuboidal in shape. These cells sometimes extended into the first alveoli evaginating from the wall. More distally in respiratory bronchioles, the walls became much more highly alveolarized (fig. 3 . ) , and the cuboidal epithelium was partially replaced by squamous epithelium. The cuboidal epithelial cells which remained in these more distal areas of respiratory bronchioles were often arranged in clusters among squamous epithelial cells (fig. 9 ) . The cuboidal cells were usually covered on their luminal surface by microvilli (fig. 10) and contained numerous mitochondria, a moderate amount of granular endoplasmic reticulum, a small Golgi complex, and occasional lysosome-like inclusions (fig. 11). In bonnet monkeys, cuboidal epithelial cells in respiratory bronchioles occasionally contained electron-dense secretory droplets. I n distal areas of respiratory bronchioles in all species, cuboidal cells were observed which contained osmiophilic lamellar bodies similar to those that are found in type I1 alveolar epithelial cells (granular pneumonocytes) (fig. 16). Capillaries were frequently observed in the walls of respiratory bronchioles immediately below the luminal epithelium (fig. 12). They were often covered by squamous epithelium and occasionally projected into the bronchiolar lumen (fig. 1 3 ) . In one stumptail monkey, we observed a cluster of cuboidal epithelial cells among which there were several cells containing densecore vesicles 75-115 n m i n diameter (fig. 14, 15). The cytoplasm of these cells resembled that of other cuboidal epithelium with the exception of the vesicles. Axons containing numerous mitochondria were

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might result in their also being found in bonnet monkeys. An unusual form of ciliated cell containing membrane-bound inclusions was often observed in bonnet monkeys (fig. 5). Although we have no histochemical information on the chemical nature of the fibrogranular material, it might be that these cells have a limited secretory function. Experimental studies are now in progress with bonnet monkeys which could provide addiDISCUSSION tional information on the composition and A number of similarities and differences function of these cytoplasmic inclusions. There are several differences between i n pulmonary airway structure were noted between macaques and man. The structure terminal bronchioles of macaques and man. In man, terminal bronchioles are of the bronchial wall in bonnet, stumptail, developed to three or four generations beand rhesus monkeys is essentially the same fore the first respiratory bronchioles are as that which has been described in m a n reached (von Hayek, '60). These airways by investigators such as von Hayek ('60) are lined for the most part by a simple and Watson and Brinkman ('64). The columnar epithelium composed of ciliated same basic cell types are found in the and nonciliated cells. The nonciliated cells bronchial wall of macaques and man, with have a prominent Golgi zone, abundant the one exception being that we did not granular endoplasmic reticulum, numerobserve nonciliated cells similar i n mor- ous mitochondria, and round homogephology to bronchial brush cells reported nously electron-dense droplets that are by Watson and Brinkman ('64). A similar apically located (Cutz and Conen, '71). intraepithelial distribution of nerves to that These nonciliated cells have been referred which we found in macaque bronchi has to in the literature as Clara cells, and are been described in man by Lauweryns et al. considered by some investigators ( Sorokin, ('70). Using electron microscopic tech- '70) to be serous secretory cells. niques and histochemical techniques for I n contrast to what has been described the detection of amines, Gmelich et al. for man, we observed that terminal bron('67), Lauweryns et aI. ('70), and Rosan chioles were only developed to a single and Lauweryns ('72) have described gran- generation in lungs from stumptail and ulated cells containing dense-core vesicles rhesus monkeys. Bronchioles were moderin bronchi and bronchioles of humans. ately longer in bonnet monkeys than in These cells have been referred to as Kult- the other two species of macaques and schitzky-like cells or AFG cells (argyrophil, occasionally divided to form secondary histochemically fluorescent, and ultrastruc- generations. Terminal bronchioles in maturally granulated). Lauweryns and Coke- caques were lined by pseudostratified colaere ('73) have presented evidence that lumnar epithelium, rather than by simple cells similar to these function i n rabbits as columnar epithelium. I n addition, whereas intrapulmonary chemoreceptor cells which nonciliated cells containing secretory dropare sensitive to hypoxic conditions. The lets, and thus being comparable to human granulated cells that we observed in the Clara cells, were observed lining bronbronchi and respiratory bronchioles of chioles of bonnet and stumptail monkeys, rhesus and stumptail monkeys had simi- no such cells were observed in any of the lar ultrastructural characteristics to the rhesus monkeys. This suggests that nonAFG cells that have been described in ciliated bronchiolar epithelial cells with a human lungs. We did not observe these merocrine secretory function are not norgranulated cells in bonnet monkeys, but mally present in rhesus lungs or that they since they were only infrequently observed are extremely scarce i n comparison to the in stumptail and rhesus monkeys, we sus- other macaques. pect that a greater sampling of tissue The general structure and number of

closely associated with the granulated epithelium (fig. 14). Alveolar ducts. Alveolar ducts (figs. 3 , 17) arose dichotomously or monopodially from respiratory bronchioles. These airways had alveoli opening along their entire length, and the walls were reduced to rings of tissue surrounding alveolar openings. They were lined by type I and type I1 alveolar epithelial cells.

INTRAPULMONARY AIRWAY MORPHOLOGY IN MACAQUES

generations of respiratory bronchioles in macaques is similar to that which has been described for m a n by von Hayek ('60). In both man and macaque, alveoli outpocket from the respiratory bronchiolar wall and increase in frequency as more distal areas or generations are reached. Cuboidal cells, although continuous in the initial portions of respiratory bronchioles, become dispersed between squamous epithelial cells in more distal areas. The cuboidal epithelial cells in respiratory bronchioles of macaques are similar to those that have been described in man by Jarkovska ('70) and Matthews and Martin ('71), except that secretory droplets are only rarely present. I n distal areas of respiratory bronchioles, cells were observed which contained osmiophilic lamellar bodies. These cells are identical in morphology to type I1 alveolar epithelial cells (granular pneumonocytes). Evidence indicates that this latter alveolar cell synthesizes pulmonary surfactant which lowers alveolar surface tension (Askin and Kuhn, '71). It could be that type I1 cells lining respiratory bronchioles have a similar function and lower surface tension in the distal airways. Von Hayek ( ' 6 0 ) , using light microscopy, reported the presence of capillaries immediately beneath the epithelium of human respiratory bronchioles. We made a similar observation i n macaques using the transmission electron microscope. This arrangement of capillaries indicates to us that there is at least a structural basis for gas exchange to occur in the bronchiolar wall. We cannot at this time, however, evaluate the extent or physiological significance of this gas exchange. In summary, the results of this study indicate that there is general similarity in the mucosal structure and degree of development of bronchi between man and macaques. Terminal bronchioles i n macaques as compared to man, however, are reduced in their overall length and extent of branching and also have a n epithelial lining which is slightly different in arrangement. Of the three macaques studied, bonnet monkeys have terminal bronchioles which most closely approach those of m a n in appearance due to their longer length

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and greater frequency of nonciliated bronchiolar epithelial cells containing electrondense secretory droplets. The mucosal structure and degree of branching of respiratory bronchioles in m a n and macaques are similar. ACKNOWLEDGMENTS

This study was supported in part by United States Public Health Service Grants RR00169 and ES00628. LITERATURE CITED Askin, F. B., and C. Kuhn 1971 The cellular origin of pulmonary surfactant. Lab. Invest, 25: 260-268. Cutz, E., and P. E. Conen 1971 Ultrastructure and cytochemistry of Clara cells. Am. J. Path., 62: 127-142. Frasca, J. M., 0. Auerbach, V. R. Parks and J. D. Jamieson 1968 Electron microscopic observations of the bronchial epithelium of dogs. I. Control dogs. Exp. Mol. Path., 9: 363-379. Freeman, G., R. J. Stephens, D. L. C o f f i and J. F. Stara 1973 Changes in dogs' lungs after long-term exposure to ozone. Light and electron microscopy. Arch. Environ. Health. 26: 209-216. Ginelich, J . T., K. G. Bensch and A. A. Liebow 1967 Cells of Kultschitzky type i n bronchioles and their relation to the origin of peripheral carcinoid tumor. Lab. Invest., 17: 88-98. Greenwood, M. F., and P. Holland 1972 The mammalian respiratory tract surface. A scanning electron microscopic study. Lab. Invest., 27: 296-304. 1973 Scanning electron microscopy of the normal and BCG-stimulated primate respiratory tract. J. Reticuloend. SOC.,13: 183-192. Gross, P., E. A. Pfitzer and T. F. Hatch 1966 Alveolar clearance: Its relation to lesions of the respiratory bronchiole. Am. Rev. Resp. Dis., 94: 10-19. Jarkovska, D. 1970 Ultrastructure of the epithelium of the respiratory bronchioles in man. Folia Morph., 18: 352-358. Karnovsky, M. J. 1965 A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J. Cell Biol., 27: 137A138A. Karrer, H. E. 1956 Electron microscopic study of bronchiolar epithelium i n normal mouse lung. Exp. Cell. Res., 10: 237-241. Krahl, V. E. 1964 Anatomy of the mammaliaii lung. In: Handbook of Physiology, section 3 : Respiration. W. 0. Fenn and H. Rahn, eds., Am. Physiol. SOC.,Washington, Vol. I, pp. 213284. Lauweryns, J . . M., and M. Cokelaere 1973 Hypoxia-sensitive neuro-epithelial bodies. Intrapulmonary secretory neuroreceptors modulated by the CNS. Z. Zellforsch., 245: 521-540. Lauweryns, J. M., J. C. Peuskens and M. Cokelaere 1970 Argyrophil, fluorescent, and granulated (Peptide and amine producing?) AFG

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cells in human infant bronchial epithelium. Light and electron microscopic studies. Life Sci., 9 ( I ) : 1417-1429. Matthews, J. L., and J. H. Martin 1971 Atlas of Human Histology and Ultrastructure. Lea and Febiger, Philadelphia, pp. 282-283. McLaughlin, R. F., W. S. Tyler and R. 0. Canada 1961 A study of the subgross pulmonary anatomy i n various mammals. Am. J. Anat., 108: 149-166. Nagaishi, C. 1972 Functional Anatomy and Histology of the Lung. University Park Press, Baltimore. Nowell, J. A., and W. S. Tyler 1971 Scanning electron microscopy of the surface morphology of mammalian lungs. Am. Rev. Resp. Dis., 103: 3 13-328. Parkinson, D. R., and R. J. Stephens 1973 Morphological surface changes in the terminal bronchiolar region of NO%-exposed rat lung. Environ. Res., 6: 37-51. Pease, D. C. 1964 Histological Techniques for Electron Microscopy. Second Edition. Academic Press, New York, pp. 38-39.

Plopper, C. G., D. L. Dungworth and W. S. Tyler 1973 Pulmonary lesions in rats exposed to ozone. A correlated light and electron microscopic study. Am. J . Path., 71: 375-394. Rhodin, J., and T. Dalhamn 1956 Electron microscopy of the tracheal ciliated mucosa i n rat. 2. Zellforsch., 44: 345-412. Rosan, R. C., and J. M. Lauweryns 1972 Mucosal cells of the small bronchioles of prematurely born human infants (600-17OOg). Beitr. Path., 147: 145-174. Sorokin, S. P. 1970 The cells of the lung. In: Morphology of Experimental Respiratory Carcinogenesis, Proceedings of Biology Division, Oak Ridge National Laboratory, P. Nettesheim, M. G. Hanna, J. W. Deatherage, eds. U. S. Atomic Energy Commission, Oak Ridge, pp. 3-43. von Hayek, H. 1960 The Human Lung. Translated by V. E. Krahl. Hafner Publishing Co., New York. Watson, J. H. L., and G. L. Brinkman 1964 Electron microscopy of the epithelial cells of normal and bronchitic human bronchus. Am. Rev. Resp. Dis., 90: 851-866.

PLATE 1 EXPLANATION OF FIGURES

1

A low power scanning electron micrograph of the end of a bronchus with cartilage in its wall (arrow) which divides into two short terminal bronchioles (TB). One of the bronchioles opens into a respiratory bronchiole (RB). Stumptail monkey. x 20.

2

This micrograph illustrates a n unusual relationship of airways that was often observed in rhesus monkeys. A bronchus with cartilage in its wall (arrow) opens directly into a respiratory bronchiole (RB), rather than into a terminal bronchiole. There is a n abrupt transition between ciliated epithelium (dark areas) in the bronchus and nonciliated epithelium (light areas) in the respiratory bronchiole. Rhesus monkey. >: 50.

3

A long respiratory bronchiole (RB) with numerous alveolar outpocketings opens into a long alveolar duct (AD) which has alveoli opening along its entire length. Rhesus monkey. x 20.

4

Ciliated and mucous cells in a bronchus. Some mucous cells project into the bronchial lumen. The outlines of underlying mucigen droplets can be seen on the surfaces of mucous cells (arrows). Rhesus monkey. x 2,500.

INTRAPULMONARY AIRWAY MORPHOLOGY I N MACAQUES W. L. Castleman, D. L. Dungworth and W. S. Tyler

PLATE 1

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PLATE 2 EXPLANATION OF FIGURES

114

5

A ciliated cell from the bronchus of a bonnet monkey. The cytoplasm includes membrane-bound material which has a fibrogranular appearance (arrow). x 9,600.

6

Ciliated and nonciliated epithelial cells lining a terminal bronchiole in a stumptail monkey. The nonciliated cells are covered by microvilli. X 2,860.

7

A nonciliated bronchiolar epithelial cell lining a terminal bronchiole in a bonnet monkey. This cell contains several round, homogenously electron-dense droplets in its apical cytoplasm. X 18,600.

IN'IRAPULMONARY AIRWAY MORPHOLOGY I N MACAQUES W. L. Castleman, D. L. Dungworth and W. S. Tyler

PLATE 2

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PLATE 3 E X P L A N A T I O N OF FIGURES

116

8

A n abrupt transition between ciliated epithelium in a terminal bronchiole and nonciliated epithelium in a respiratory bronchiole. This is a high magnification field of a n area of transition similar to that which is illustrated in figure 2. Rhesus monkey. x 420.

9

The wall of a well-developed respiratory bronchiole and nearby alveoli (A). The cuboidal cells are not as densely grouped together as in more proximal areas of respiratory bronchioles and are often arranged in clusters (arrow) between squamous epithelium. Stumprail monkey. x 800.

10

Cuboidal epithelium lining a respiratory bronchiole. These cells are covered over their entire surface by microvilli. Rhesus monkey. )i. 5,000.

11

Portions of two cuboidal cells lining a respiratory bronchiole. These cells contain numerous mitochondria, a small Golgi complex, a moderate amount of granular endoplasmic reticulum, but usually do not contain secretory droplets. Stumptail monkey. )i. 7,900.

INTRAPULMONARY AIRWAY MORPHOLOGY IN MACAQUES W. L. Castleman, D. L. Dungworth and W. S. Tyler

PLATE 3

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PLATE 4 EXPLANATION OF FIGURES

118

12

A capillary ( C ) is positioned close to the basal surface of the lining epithelium of a respiratory bronchiole. Smooth muscle is located in the bottom of the field and cuboidal epithelium lines the wall of the bronchiole. Rhesus monkey. x 4,000.

13

A portion of a respiratory bronchiolar wall. A capillary ( C ) covered by flattened epithelium projects into the bronchiolar lumen almost to the top level of the cuboidal epithelium. Rhesus monkey. 7,300.

INTRAPULMONARY AIRWAY MORPHOLOGY IN MACAQUES W. L. Castleman, D. L. Duiigworth and W. S. Tyler

PLATE 4

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PLATE 5 EXPLANATION O F F I G U R E S

14 A n axon (arrow) containing many mitochondria is associated with granulated cells in the mucosa of a respiratory bronchiole. Stumptail monkey. x 10,200.

15

A high magnification field of the granules shown in the epithelial cells of the preceding figure. These granules are in the form of densecore vesicles, 75-115 n m in diameter. Stumptail monkey. x 57,700.

16

A cuboidal cell which was often observed in distal areas of respiratory bronchioles. This cell contains osmiophilic lamellar bodies (arrow) and is identical in appearance to a type I1 alveolar epithelial cell. Rhesus monkey. x 8,300.

17 A n alveolar duct and surrounding alveolar parenchyma. Alveoli open along the entire length of the alveolar duct. Rhesus monkey. x 65.

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INTRAPULMONARY AIRWAY MORPHOLOGY IN MACAQUES W. L. Castleman, D. L. Dungworth and W . S. Tyler

PLATE 5

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Intrapulmonary airway morphology in three species of monkeys: a correlated scanning and transmission electron microscopic study.

Intrapulmonary Airway Morphology in Three Species of Monkeys : A Correlated Scanning and Transmission Electron Microscopic Study W. L. CASTLEMAN, D. L...
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