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Respiratory apparatus
Respiratory apparatus M. Navarro, J. Ruberte and A. Carretero
The respiratory apparatus is formed by two major functional parts, respiratory tracts or airways, which are responsible for conducting the air, and the respiratory part, where gasses are exchanged, principally the release of carbon dioxide and the uptake of oxygen. For the anatomical description, we will use the human classical terms «upper» respiratory tract and «lower» respiratory tract. The upper respiratory tract includes the organs located within the skull, that are, nasal cavities, paranasal sinuses and nasopharynx, whereas the lower respiratory tract consists of the larynx, trachea and lungs. The airways are responsible not only for conducting the air, but also for conditioning the temperature and moisture of the inspired air, as well as removing impurities. In addition, the airways have important functions such as olfaction and phonation, and they are related with sexual behavior.
■ ■ NASAL CAVITY There are two nasal cavities or nasal fossas, which are symmetrical and separated by the nasal septum. The openings of these cavities are the nasal orifices, also known as nares or nostrils, which are located at the tip or apex of the nose. The external nose is supported only by cartilage and covered by a modified skin called the nasal plate (Fig. 6-1). The nasal cavities are bounded by the nasal bones, the incisive bones and the maxillae. The cribriform plate of the ethmoid bone and the choanae, the bone orifices which communicate with the nasopharynx, are the caudal limit of nasal cavities. The nasal septum consists of a bony part (the perpendicular plate of the ethmoid bone and the vomer) and a cartilaginous part (the cartilage of the nasal septum) lying on the vomer. In addition, on its rostral part, the mouse also has a membranous part (Fig. 6-3) that facilitates the mobility of the external nose. In mice the nasal septum is not complete because, just before entering into the nasopharynx, it presents a small communication between both nasal fossas which is referred to as the window of the nasal septum (Fig. 6-16). This window has also been described in rats, hamsters and guinea pigs, and in nasal instillation experiments with these species, each nasal cavity cannot be treated individually. At this level, the mouse has focal aggregates of nasal-associated lymphoid tissue (NALT). Because of their strategic position at the entrance of nasopharyn-
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geal meatus, these mucosal lymphoid aggregates have an important role in regional immune response. NALT has been considered to be the homolog of the human tonsil. The nasal cavity is structurally and functionally a complex. In its interior the nasal cavity has the conchae, which are spiral bone laminas coated with mucosa. The mouse has two nasal conchae, the dorsal nasal concha and the ventral nasal concha, which are analogues of the superior and inferior nasal conchae of man, as well as the ethmoid conchae which are known as ethmoturbinates (Fig. 6-3). In mice, the dorsal nasal concha is part of the nasal bone, while the ventral nasal concha is part of the incisive bone, which is different from what is seen in most animal species (Fig. 6-4). The ethmoturbinates are delicate osseous scrolls of the ethmoid bone in the caudal part of the nasal cavity, and because of their complex structure they are also called collectively as the ethmoidal labyrinth (Figs. 6-2 and 6-3). The mouse has four major ethmoid conchae, also known as endoturbinates (I-IV), which extend far into the nasal cavity, and a series of smaller and more superfi cial conchae denominated as ectoturbinates located between them (Figs. 6-3, 6-14 and 6-17). The spaces between the conchae are called meatuses. The dorsal nasal meatus is the space located dorsally to the dorsal nasal concha. The ventral nasal meatus is the space between the ventral nasal concha and the floor of the nasal cavity and is the only one that communicates caudally with the nasopharynx via the nasopharyngeal meatus. The space between the dorsal and ventral nasal conchae is the middle nasal meatus whereas the common nasal meatus is the name given to the space between the nasal septum and conchae. Finally, the spaces between the ethmoturbinates are called the ethmoidal meatuses (Figs. 6-4 and 6-13). The entire nasal cavity is lined by different kinds of epithelia which determine three different regions. The ventral part of the vestibule or entrance of the nasal cavity is the cutaneous region lined by a squamous epithelium similar to the epithelium of the external nose. It is a stratified epithelium composed of basal cells and several layers of squamous cells that become progressively more flattened towards the surface (Fig. 6-5). The nasal conchae, and most of the nasal septum and the walls of the nasal cavity are lined with respiratory epithelium and therefore collectively they are referred as the respiratory region. The
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typical respiratory epithelium is a pseudostratified ciliated columnar epithelium, more or less columnar depending on the area, composed by ciliated, non-ciliated and basal cells. In mice, the typical respiratory epithelium can be found lining the medial part of the nasal conchae and the central part of the nasal septum (Fig. 6-6). In some areas, especially in the ventral part of the nasal septum, the respiratory epithelium has numerous goblet cells which produce mucin (Fig. 6-7). In humans, there is a gradual rostrocaudal increase in the number of goblet cells in the nasal cavity. In other areas of the nasal cavity, the mouse presented the transitional respiratory epithelium. This type of epithelium is lining the lateral part of the nasal conchae and in the lateral part of the nasal meatuses. This epithelium is composed of cuboidal ciliated cells and interspersed cuboidal non-ciliated cells (Fig. 6-8). Below the respiratory epithelium is found the lamina propria formed by collagen cells, blood vessels, nerves, nasal glands and a well-developed nasal cavernous plexus. This venous cavernous plexus expands or contracts depending on temperature, humidity and carbon dioxide concentration in the inspired air. Summarizing, the respiratory mucosa is responsible for conditioning the inspired air, it removes impurities through the cilia, it humidifi es air by evaporation of mucus, and it heats air through heat exchange with the blood of the cavernous plexus. These functions are particularly important in animals like mice because all the inspired air enters through the nasal cavity. To complete the nasal cavity epithelial lining there is an olfactory region located caudally. In the mouse, the ethmoturbinates and dorsal nasal meatus are covered by olfactory epithelium. This epithelium is similar to humans and consists of sustentacular cells, which are columnar secretory cells with microvilli, neurosensory olfactory cells arranged in five or six layers, and basal cells (Fig. 6-15 and 13-39). The olfactory neurosensory cells are bipolar neurons with dendritic process that terminate as olfactory vesicle in the apical part of the epithelium. These olfactory vesicles have several radiate non-motile cilia that are receptive for different varieties of scents. The axon of olfactory neurosensory cells extends towards the basal part of the epithelium to form unmyelinated nerves, the olfactory nerves, which make synapses with neurons in the olfactory bulb. In addition to these nerves, blood vessels and the olfactory glands, or Bowman’s glands, can also be found in the lamina propria of the olfactory mucosa (Fig. 6-15 and 13-39). The olfactory glands are simple tubule-alveolar glands whose secretion moistens the mucosa and acts as a solvent for olfactory stimuli. The ratio of the three types of epithelium in mice is approximately 7 % squamous epithelium, 46 % respiratory epithelium and 47 % olfactory epithelium, but can vary with age and mouse strain. The proportion of olfactory epithelium in mice is much higher than in man (about 3 %). The nasal epithelium is susceptible to injury, especially from inhaled toxics. For routine examination in toxicological or carcinogenic studies, standardized cross
sections of the nasal cavity in at least three levels should be analyzed. Level 1 is a transverse section made caudally to the superior incisor teeth (Fig. 6-4), level 2 a transverse section made caudally to the incisive papilla (Fig. 6-13) and level 3 a transverse section made through the second superior molar tooth (Fig. 6-14). The nasolacrimal duct can be observed in the rostral sections of the nasal cavity. This duct originates within the lacrimal sac, at the medial angle of the eye. From there, the most caudal part of the nasolacrimal duct is located laterally to the root of the incisor tooth (Fig. 6-13), it then runs along the ventral part of the tooth (Fig. 6-12) and finishes in a medial position in relation to the tooth (Fig. 6-4), where it empties ventromedially to the nasal cavity. The mouse nasolacrimal duct has a large diameter, is lined by stratifi ed squamous epithelium and is surrounded by the nasal cavernous plexus, which is especially developed in the caudal part of the duct (Fig. 6-13). The mouse has a well-developed vomeronasal organ (Jacobson’s organ) located in the rostral part of the nasal cavity. This organ is composed of two caudally blindended epithelial tubes, the vomeronasal ducts which open into the nasal vestibule through a narrow duct. The vomeronasal organ is located on either side of the nasal septum. In most species, this organ is enclosed by a cartilaginous capsule. However, in mice it present a osseous capsule, the vomeronasal bone, is a dilatation of the rostral part of the vomer (Fig. 6-9). The vomeronasal duct is lined by two types of epithelium (Fig. 6-10). Its medial wall is lined with a crescent-shaped sensory epithelium that is similar to the olfactory epithelium. However, its bipolar neurons, are without cilia and the sustentacular cells have an oval nuclei. From this sensory epithelium emerges the vomeronasal nerve which will form synapses in the accessory olfactory bulb. The lateral wall of the vomeronasal duct is formed by a non-sensory ciliated columnar epithelium. A large blood vessel runs laterally to the vomeronasal duct (Figs. 6-10 and 6-11). Changes in blood flow within this vessel influence the arrival of stimuli to the vomeronasal organ. This organ is able to collect non-volatile odoriferous stimuli (pheromones) from biological fluids such as urine, skin secretions or saliva. Pheromones play a crucial role in both reproductive physiology and sexual behavior. The vomeronasal organ forms part of the accessory olfactory system. In humans, the vomeronasal organ is a vestigial organ and, although it has been described in both development and adulthood, its functionality is far from clear. Located ventrally to the vomeronasal organ are the incisive ducts which are a communication between nasal and oral cavities (Fig. 6-12). These ducts are lined by stratified squamous epithelium as a continuation of the nasal vestibule epithelium. They originate independently from the two nasal fossas and open in two orifices located laterally in the incisive papilla of hard palate. Unlike other animal species and man, the mouse only has a single paranasal sinus, the maxillary sinus. This sinus is voluminous and mainly located above the zygo-
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matic arch (Fig. 6-16 and 6-17). Its rostrodorsal part communicates with the ethmoid labyrinth. The middle part of the sinus communicates with caudal part of the middle nasal meatus through the nasomaxillary opening. The maxillary sinus ends as a caudal recess at the level of the fi rst upper molar tooth (Fig. 6-17). The epithelium lining the sinus is a typical ciliated respiratory epithelium. Surrounding the maxillary sinus there are two nasal glands; the lateral nasal gland and the maxillary gland. These two glands are mixed glands and morphologically difficult to distinguish although they do show very different affinities for PAS staining (Fig. 6-16). The lateral nasal gland (Steno’s gland) surrounds the rostral and ventrolateral part of the sinus, and empties through a large excretory duct (Fig. 6-4) at the entrance of the nasal cavity. The maxillary gland surrounds the rest of the maxillary sinus, and drains directly into the sinus through small excretory ducts. The mouse has other smaller nasal glands including the anterior glands and the posterior glands of the nasal septum, which are located in the dorsal and ventral part of the septum, respectively. Whereas the anterior glands have the appearance of mucous glands, the posterior glands are of a serous aspect and PAS-positive (Fig. 6-11). The excretory ducts of the anterior glands open into the nasal vestibule. The posterior glands of the nasal septum are partially located within the vomeronasal bone. Because of this, they are also named as vomeronasal glands. These glands empty their secretions into the vomeronasal duct. Two excretory ducts can be seen in the junctions between the sensory and non-sensory epithelium of vomeronasal ducts (Fig. 6-11). The blood supply of mouse nasal cavity comes from different arteries (Fig. 6-18). The major palatine artery passes through the major palatine foramen and sends branches to the hard palate and the rostral region of the nose. The sphenopalatine artery passes through the foramen of the same name to enter and vascularize the nasal cavity. The external ethmoidal artery, a branch of the ophthalmic artery, enters through the ethmoidal foramen to vascularize the ethmoturbinates. All these arteries arise from the maxillary artery. In addition, the internal ethmoidal arteries arrive to the nasal cavity passing through the cribriform plate of the ethmoid bone. The internal ethmoidal arteries, which are branches of the rostral cerebral arteries, supply the most of the nasal conchae and nasal septum, unlike other animal species where the main blood supply for the nasal cavity arrives from the external ethmoidal arteries.
■ ■ LARYNX After passing through the nasal cavity and nasopharynx, inspired air enters the larynx. The larynx is a tubeshaped musculocartilaginous organ whose main function is to let the air pass from the pharynx to the trachea, preventing aspiration of food or any other foreign material into the lower respiratory tract. In addition, the larynx is the organ of phonation.
The mouse larynx, as in all domestic mammals, consists of three unpaired cartilages: the epiglottic cartilage, the thyroid cartilage and the cricoid cartilage, and two arytenoid cartilages (Fig. 6-19). The epiglottic cartilage forms the epiglottis which opens and closes the laryngeal inlet. The thyroid cartilage, is formed by a double lamina in form of a «U» opened dorsally. The thyroid cartilage articulates caudally with the cricoid cartilage, a closed ring-shaped cartilage which is composed of a ventral arch and a dorsal lamina. Within the thyroid cartilage, and articulating caudally with the cricoid cartilage, are located the arytenoid cartilages. They are hook-shaped and their corniculate processes are separated into two little cartilages in humans (corniculate cartilages). The laryngeal inlet is an orifi ce delimits the epiglottis, the corniculate tubercles (corniculate processes covered by mucosa) and the aryepiglottic folds (Fig. 6-22). Upon entering the laryngeal cavity, the vestibule of the larynx is found. There the mouse has an enormous median laryngeal recess (Figs. 6-22 and 6-23). The caudal limit of the vestibule of the larynx are the vocal folds or vocal cords, which are produced by the prominence of vocal muscles. The mouse, unlike humans and other animal species, have no vestibular folds or false vocal cords. The glottis consist of the paired arytenoid cartilages dorsally and the paired vocal folds ventrally. The narrow space left between the vocal folds is the rima glottidis or glottic cleft (Fig. 6-23). As air passes, vibration of the vocal folds occurs and, depending on their degree of contraction, the mouse emits different types of sounds, although most are in an ultrasonic range. Caudal to the glottis the lumen of larynx becomes wider. This short part of the larynx is called the infraglottic cavity, which is continuous with the trachea. The epithelium lining the laryngeal inlet is like the epithelium of the oropharynx, a stratified squamous columnar epithelium. Caudally to this it becomes pseudostratifi ed, and returns to be a ciliated columnar respiratory epithelium in the infraglottic cavity. The areas of transition between the different epithelia, such as between the base of the epiglottis and the median laryngeal recess, are very sensitive to damage from inhaled toxic or irritating agents. In the submucosa of the larynx, the mouse has some well-developed laryngeal glands. They are mixed glands, but with predominance of mucous or serous glands depending on the region. Can be distinguished one epiglottic gland (Fig. 6-22) and several laryngeal glands between the cricoid cartilage and the first tracheal cartilage (Fig. 6-24). In all mammals, a set of bones called the hyoid bone or hyoid apparatus (Figs. 6-20 and 6-21), is responsible for fixing the larynx and tongue to the base of the cranium, articulating with the thyroid cartilage of the larynx and the temporal bone. The mouse hyoid bone is similar to humans and is attached to the larynx and cranium only by ligaments and muscles. It has an unpaired transversal bone, the basihyoid (body), and two paired bones, the ceratohyoids (lesser horns) and the thyrohyoids (greater
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horns). The ceratohyoid is more rostral and highly developed in the mouse, joining with the temporal bone by the stylohyoid ligament. The thyrohyoid binds the thyroid cartilage through the thyrohyoid ligaments.
■ ■ TRACHEA The trachea is a cartilaginous tube formed by a series of tracheal cartilages, joined together by annular ligaments (Figs. 4-13, 4-15 and 6-9). These cartilages give the trachea rigidity and prevent its collapse. In the mouse, the trachea has about 15 cartilages with an approximate internal diameter of 1.5 mm. The C-shaped cartilages are open dorsally. The dorsal space is bridged by connective tissue and the tracheal muscle, a smooth muscle that is responsible for contracting the lumen of the trachea (Fig. 6-24). The trachea extends from the cricoid cartilage of the larynx to its bifurcation into two main bronchi (Fig. 6-27). The trachea is divided into a cervical part situated in the ventral region of the neck, and a thoracic part inside the thorax. The epithelial lining of the trachea is a pseudostratified columnar respiratory epithelium consisting of ciliated and clara cells. The proportion of clara cells is increased in the caudal part of the trachea, and goblet cells are only found rarely. The location of clara cells in the trachea is unique to the mouse since these cells are only found in the caudal part of airways of most species. There are tracheal glands in the submucosa, although they are restricted to the craneal part of the trachea in the mouse (Fig. 6-24).
■ ■ LUNGS The left and right lungs are two elastic organs that occupy most of the thoracic cavity (Figs. 6-25 and 6-26). In the mouse, the total lung capacity is about 1 ml. The left lung of the mouse is smaller and, unlike what happens in other animal species or humans, it is not divided. The right lung has four lobes; cranial, middle, caudal and accessory lobes (Figs. 6-25 to 6-29). Each lung has a costal surface, in contact with the thoracic wall; a medial surface, which contacts the vertebrae and mediastinum; and a diaphragmatic surface on the caudal portion of the lung in contact with the diaphragm. In addition, the right lung has interlobular surfaces between the different lobes. On the medial surface is the hilus of the lung, which is the area where the bronchi, vessels and nerves enter and leave the lung. The collective name for these structures is the root of the lung (Fig. 6-29). In the hilus of the lung, the visceral pleura that covers the lung folds and continues as the parietal pleura, which lines the walls of the thoracic cavity and the mediastinum. The pleural cavity is situated between the visceral and parietal pleurae. There are two independent pleural cavities, one for each lung, containing only a thin film of fluid to reduce friction during respiration. The space between the right and the left pleural cavities is the mediastinum, in which the heart and other thoracic organs, mainly the great vessels, nerves and esophagus are situated.
The bronchial tree begins when the trachea divides into the two left and right main bronchus (Figs. 6-26 to 6-29). In the interior of the bifurcation there is a crest known as the carina tracheae that marks the separation of the two main bronchi. These continue surrounded by bronchial cartilages, which disappears once the bronchus enters in the lungs (Fig. 6-29). Bronchial cartilages is replaced by smooth muscle. Within the lung, the right main bronchus divides into several lobular bronchi, one for each lobe. The lobular bronchi branch further, going in different directions as segmental bronchi (Fig. 6-30) that ventilate the bronchopulmonary segments into which the lung parenchyma is divided. In turn, the segmental bronchi branch into bronchioles, of a similar structure to the last ones, but of smaller diameter and ending in the terminal bronchioles. The mouse has large airways, representing a greater percentage of the total lung volume compared to other species. Usually, the mouse has no respiratory bronchioles and the terminal bronchioles often divide directly into the alveolar ducts (Fig. 6-31). The respiratory epithelium of the bronchial tree is a simple epithelium that is transformed from columnar to cuboidal. The epithelium of the intrapulmonary airways has no basal cells and is formed by ciliated cells, occasional neuroendocrine cells and a large number of secretory cells, the clara cells (Fig. 6-30). Clara cells have an irregular form and the nucleus is situated at the base of the cell with abundant agranular endoplasmic reticulum and numerous electron-lucid secretory granules in the apical cytoplasm. The granules are mainly glycoproteins that help degrade toxins, protect the epithelium and reduce surface tension. In most species, including humans, these cells are only found in the bronchioles. However, in the mouse they can be found from the trachea down, further increasing in the more distal portions, and representing about 60 % of the epithelial cells of the bronchial tree. Other cells like serous cells or brush cells are rare in intrapulmonary bronchi and bronchioles of mice. It is in the respiratory part (gas exchange area) or lung parenchyma (Fig. 6-31) where gas exchange occurs. Here, the terminal bronchioles branch into the alveolar ducts which open into the alveolar sacs. The alveolar sacs are groups of pulmonary alveoli shaped as a bunch of grapes. These alevoli are small in mice (40 - 80 microns) compared to those of other species. The alveoli are supported by interstitial tissue with abundant elastic tissue, collagen and numerous capillaries. The epithelium of the alveolus is composed of two types of pneumocytes. Type I or respiratory pneumocytes are elongated flat cells. Their cytoplasm together with a dual basement membrane and the endothelial cell cytoplasm form the wall of the alveolus (the blood-air barrier) (Fig. 6-31), where gas exchange occurs. Type II or granular pneumocytes are found between the interalveolar septa and contain lamellar bodies that give them the granular appearance. These lamellar bodies produce phospholipid-rich surfactant required to reduce the surface tension in the alveoli. Only Type II
6. Respiratory apparatus
pneumocytes have mitotic capacity and moreover, they also are able to differentiate into type I cells. The main function of the lungs is to oxygenate blood. The blood reaches the lungs via the left and right pulmonary arteries (Fig. 11-22), which will continue branching as does the bronchial tree, down into the capillaries which are tightly related to the alveoli of the lung. However, in the mouse the segmental arteries do not accompany the segmental bronchi, but instead run between the bronchopulmonary segments (Fig. 6-33). This situation is opposite to that which occurs in man, where the segmental arteries accompany the segmental bronchi. The blood, once oxygenated, returns through the pulmonary veins (Fig. 11-22) to the heart following the same pattern of branching and
accompanying the bronchial tree (Fig. 6-33). In addition to this pulmonary circulation (functional), there is a bronchial circulation (nutritional) that comes from branches from the thoracic aorta and the intercostal arteries. In the mouse, there is controversy about whether this vascularization reaches the alveolar level as in other species, or if it only nourishes the trachea and the main bronchi without penetrating into the lung parenchyma. With respect to the lymph nodes, the mouse has only one right tracheobronchial lymph node, located cranially to the origin of the right main bronchus and it may have small pulmonary lymph nodes within the lung parenchyma (Fig. 6-29). Bronchiole associated lymphoid tissue (BALT) is rarely observed in the lungs of healthy mice.
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Figure 6-2. Nasal cavity. Sagittal sections. A) Topography of nasal cavity in a median section of head. B) Scanning electron microscopy image of one week old mouse (P7). Roman numerals indicate the number of endoturbinates. 1: Dorsal nasal concha; 2: Ventral nasal concha; 3: Endoturbinates; 4: Cribriform plate (ethmoid bone); 5: Straight fold; 6: Basal fold; 7: Dorsal nasal meatus; 8: Middle nasal meatus; 9: Ventral nasal meatus; 10: Ethmoidal meatuses; 11: Hard palate; 12: Brain; 13: Larynx; 14: Incisive bone; 15: Nasal bone; 16: Nasomaxillary opening.
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Figure 6-3. Nasal cavity. A) Nasal septum. Median section. One week old mouse (P7). B) Lateromedial radiography of a half skull. C) Bones of nasal cavity. Median section of skull. D) Detail of ethmoidal labyrinth (ethmoturbinates). Perpendicular plate of ethmoid bone, nasal bone and dorsal nasal concha were removed. Roman numerals indicate the number of endoturbinate. 1: Membranous part of nasal septum; 2: Cartilagenous part of nasal septum; 3: Perpendicular plate (ethmoid bone); 4: Dorsal nasal concha; 5: Vomeronasal bone; 6: Endoturbinates; 7: Middle nasal meatus; 8: Ventral nasal meatus; 9: Ectoturbinates; 10: Ethmoidal meatuses; 11: Nasal bone; 12: Incisive bone; 13: Maxilla; 14: Zygomatic process; 15: Vomer; 16: Upper incisor tooth; 17: Dental alveolus of upper incisor tooth; 18: Basal plate (floor of ethmoidal labyrinth); 19: Cribriform plate (ethmoid bone); 20: Ethmoidal foramen; 21: Sphenopalatine foramen; 22: Upper molar teeth; 23: Nasopharyngeal meatus; 24: Nasomaxillary opening.
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20 Figure 6-4. Transverse section of nasal cavities. Level 1. A) Localization of epithelia in nasal cavity. The different types of respiratory epithelia (6, 7 and 8 squares) are showed in corresponding images on the next page. Histological section. Masson’s trichrome stain (20X). B) Computed tomography image. 1: Stratified squamous epithelium; 2: Olfactory epithelium; 3: Dorsal nasal concha; 4: Ventral nasal concha; 5: Nasolacrimal duct; 6, 7 and 8: Respiratory epithelium; 9: Cartilage of nasal septum; 10: Vomeronasal bone (vomer); 11: Vomeronasal organ; 12: Root of upper incisor tooth; 13: Dorsal nasal meatus; 14: Middle nasal meatus; 15: Ventral nasal meatus; 16: Common nasal meatus; 17: Nasal vestibule; 18: Incisive bone; 19: Nasal bone; 20: Palatine fissure; 21: Anterior gland of nasal septum; 22: Posterior gland of nasal septum; 23: Lateral nasal gland; 24: Excretory duct of lateral nasal gland; 25: Nasal cavernous plexus.
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Figure 6-5. Stratified squamous epithelium. A) Hematoxylin-eosin stain (1,000X). B) Staining with Lycopersicon esculentum lectin revealed by DAB (brown) and hematoxylin (1,000X). 1: Squamous cells; 2: Basal cells; 3: Lamina propria.
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Figure 6-6. Respiratory ciliated columnar epithelium. Magnification of square 6 in figure 6-4 (A). (1,000X). A) Hematoxylin-eosin stain. B) Staining with Lycopersicon esculentum lectin revealed by DAB (brown) and hematoxylin. 1: Ciliated columnar cells; 2: Basal cells; 3: Lamina propria; 4: Nasal cavernous plexus.
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Figure 6-7. Respiratory epithelium with abundant goblet cells. Magnification of square 7 in figure 6-4 (A). (1,000X). A) Hematoxylin-eosin stain. B) Staining with Lycopersicon esculentum lectin revealed by DAB (brown) and hematoxylin. 1: Ciliated columnar cells; 2: Basal cells; 3: Lamina propria; 4: Nasal cavernous plexus; 5: Caliciform mucosal cells (globet cells); 6: Capillary.
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5 Figure 6-8. Transitional respiratory epithelium. Magnification of square 8 in figure 6-4 (A). (A8) (1,000X). A) Hematoxylineosin stain. B) Staining with Lycopersicon esculentum lectin revealed by DAB (brown) and hematoxylin. 1: Non-ciliated cuboidal cells; 2: Basal cells; 3: Ciliated cuboidal cells; 4: Lamina propria; 5: Lateral nasal gland; 6: Capillary.
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14 Figure 6-9. Location of vomeronasal organ. A) Dorsal view of nasal cavities. Nasal bones and dorsal nasal conchae were removed. B) Detail after removing ventral nasal conchae. C) Ventral view of nasal cavities. D) Dorsoventral radiography of nasal cavities. E) Computed tomography image. Horizontal section of nasal cavities.
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1: Vomeronasal bone; 2: Vomer; 3: Incisive bone; 4: Dental alveolus of upper incisor tooth; 5: Upper incisor tooth; 6: Maxilla; 7: Zygomatic process (maxilla); 8: Ventral nasal concha; 9: Ethmoturbinates; 10: Endoturbinate I; 11: Endoturbinate II; 12: Perpendicular plate (ethmoid bone); 13: Interincisive fissure; 14: Palatine fissure; 15: Palatine process (maxilla); 16: Vomeromaxillary suture (between vomeronasal bone and palatine process of maxilla); 17: Nasolacrimal duct; 18: Maxillary sinus; 19: First upper molar tooth.
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Figure 6-10. Structure of vomeronasal organ. Transverse sections. A) Histological section. Hematoxylin-eosin stain (100X). B) Magnetic resonance image of nasal cavity (level 1). C) Ultrasound image. D) Staining with Lycopersicon sculentum lectin revealed by DAB (brown) and hematoxylin (100X). E and F) Magnifications of sensory and non-sensory epithelia, respectively (1,000X). 1: Vomeronasal bone (vomer); 2: Sensory epithelium; 3: Non-sensory epithelium; 4: Vomeronasal duct; 5: Blood vessel of vomeronasal organ; 6: Lamina basal; 7: Capillary; 8: Vomeronasal nerve; 9: Posterior gland of nasal septum; 10: Cartilage of nasal septum; 11: Respiratory epithelium; 12: Nasal cavernous plexus; 13: Ventral nasal meatus; 14: Nasal bone; 15: Skin; 16: Dorsal nasal concha; 17: Ventral nasal concha; 18: Nasolacrimal duct; 19: Root (dental pulp) of upper incisor tooth; 20: Neurosensory olfactory cells; 21: Sustentacular cell; 22: Ciliated columnar cell; 23: Basal cells.
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Figure 6-13. Transverse section of nasal cavity. Level 2. A) Masson’s trichrome stain (20X). B) Computed tomography image. C) Detail of nasolacrimal duct epithelium. Hematoxylin-eosin stain (1,000X). 1: Nasal bone; 2: Incisive bone; 3: Cartilage of nasal septum; 4: Vomer; 5: Vomeronasal bone (vomer); 6: Blood vessel of vomeronasal organ; 7: Nasal cavernous plexus; 8: Dorsal nasal concha; 9: Ventral nasal concha; 10: Root of upper incisor tooth; 11: Dental alveolus of upper incisor tooth; 12: Nasolacrimal duct; 13: Dorsal nasal meatus; 14: Common nasal meatus; 15: Ventral nasal meatus; 16: Olfactory epithelium; 17: Palatine fissure; 18: Palatine mucosa; 19: Oral cavity; 20: Squamous cells; 21: Basal cell; 22: Lamina propria.
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Figure 6-14. Transverse section of nasal cavities. Level 3. A) Masson’s trichrome stain (20X). B) Computed tomography image. 1: Frontal bone; 2: Second upper molar tooth; 3: Maxilla; 4: Perpendicular plate (ethmoidal bone); 5: Nasopharyngeal meatus; 6: Nasal associated lymphoid tissue (NALT); 7: Hard palate; 8: Palatine mucosa; 9: Palatine raphe; 10: Major palatine artery (inside major palatine canal); 11: Ectoturbinates; 12: Endoturbinate III; 13: Endoturbinate IV; 14: Olfactory bulb; 15: Olfactory nerves; 16: Lacrimal gland of third eyelid (Harderian gland).
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Figure 6-17. Maxillary sinus. Computed tomography images (A-E) and magnetic resonance images (F and G). A) Sagittal section of nasal cavity indicating planes of transverse sections. B) Communication with ethmoidal labyrinth. C) Communication with nasal cavity. D) Maxillary sinus at level of zygomatic process. E) Caudal recess of maxillary sinus. F) Sagittal section of nasal cavity showing reference of transverse section. G) Maxillary sinus at level of zygomatic process.
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Figure 6-18. Arterial vascularization of nasal cavity. A) Arterial injection with Araldit® (red). Soft tissue was macerated with pancreatin. Nasal bone, incisive bone, maxilla and mandible of left side were removed. B) Arterial injection with latex (green). Alizarin red stained and clearing. Horizontal section. 1: Nasal bone; 2: Incisive bone; 3: Mandible; 4: Maxilla; 5: Frontal bone; 6: Cribriform plate (ethmoidal bone); 7: Eyeball; 8: Lacrimal gland of third eyelid (Harderian gland).; 9: Dorsal nasal concha; 10: Ventral nasal concha; 11: Ethmoturbinates; 12: Vomeronasal bone; 13: Ethmoidal foramen; 14: Sphenopalatine foramen (opened); 15: Maxillary artery (through alar canal); 16: Ophtalmic artery; 17: Infraorbital artery; 18: Sphenopalatine artery; 19: Major palatine artery; 20: Septal nasal artery; 21: External ethmoidal artery; 22: Ethmoidal branch; 23: Internal ethmoidal arteries; 24: Caudal lateral nasal artery; 25: Caudal septal nasal artery.
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Figure 6-19. Topography of larynx and laryngeal cartilages. A) Median section of head. B) Magnetic resonance image. C) Ventral view of neck. M. sternohyoideus and salivary glands were removed. D) Ventral view of laryngeal cartilages. E) Dorsal view of laryngeal cartilages. 1: Nasal cavity; 2: Brain; 3: Spinal cord; 4: Tongue; 5: Hard palate; 6: Soft palate; 7: Nasopharynx; 8: Oropharynx; 9: Basihyoid; 10: Larynx; 11: Trachea; 12: M. sternohyoideus; 13: M. masseter; 14: M. mylohyoideus; 15: M. sternomastoideus; 16: M. pectoralis superfi cialis; 17: External acoustic meatus; 18: Thyroid gland; 19: Cricothyroid ligament; 20: Anular ligament; 21: Tracheal cartilage; 22: Epiglottic cartilage; 23: Thyroid cartilage; 24: Arytenoid cartilages; 25: Cricoid cartilage; 26: Left lamina (thyroid cartilage); 27: Right lamina (thyroid cartilage); 28: Laryngeal prominence; 29: Caudal thyroid notch; 30: Caudal horn (thyroid cartilage); 31: Cricothyroid joint; 32: Corniculate process (arytenoid cartilage); 33: Arch of cricoid cartilage; 34: Lamina of cricoid cartilage.
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Figure 6-24. Topography and structure of trachea. A and B) Transverse histological sections. Hematoxylin-eosin stain (40X). C) Ultrasound image of trachea. Sagittal section. D) Respiratory epithelium of trachea. Hematoxylin-eosin stain (1,000X). 1: Lamina of cricoid cartilage; 2: Arch of cricoid cartilage; 3: Tracheal cartilage; 4: Esophagus; 5: M. cricoarytenoideus dorsalis; 6: Thyroid gland; 7: M. trachealis; 8: Laryngeal gland; 9: Tracheal gland; 10: Mandibular gland; 11: M. sternohyoideus; 12: Ciliated columnar cell; 13: Clara cell; 14: Basal cells; 15: Lamina propria.
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Figure 6-25. Topography of lungs. A) Computed tomography image. 3D reconstruction. Left lateral view. B) Laterolateral broncography. C) Lateral view of left lung. Left thoracic limb and muscles of thoracic wall were removed. 1: Trachea; 2: Lung; 3: First rib; 4: Eighth rib; 5: Sternum; 6: Axis; 7: Pleural cupula; 8: Mm. intercostales (partially removed); 9: Epaxial muscles; 10: M. pectoralis profundus; 11: M. rectus abdominis.
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Figure 6-26. Topography of lungs. A) Computed tomography image. 3D reconstruction. Dorsal view. B) Thoracic cavity dorsally opened. C) Dorsoventral broncography. D) Magnetic resonance image. Horizontal Section. 1: Left lung; 2: Right lung; 3: Cranial lobe (right lung); 4: Middle lobe (right lung); 5: Caudal lobe (right lung); 6: Accessory lobe (right lung); 7: Diaphragm; 8: Esophagus (thoracic part); 9: Thoracic aorta; 10: Trachea; 11: Left main bronchus; 12: Right main bronchus; 13: Left pulmonary artery and vein; 14: Caudal vena cava; 15: Cranial lobar bronchus; 16: Liver; 17: Stomach.
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Figure 6-27. Lobes of lungs. Araldit® airway cast. A) Dorsal view. B) Ventral view. C) Caudal view (diaphragmatic surface). 1: Left lung; 2: Cranial lobe (right lung); 3: Middle lobe (right lung); 4: Caudal lobe (right lung); 5: Accessory lobe (right lung); 6: Trachea; 7: Left main bronchus; 8: Right main bronchus; 9: Apex of lung; 10: Cranial interlobular fissure; 11: Caudal interlobular fissure; 12: Hilus of lung; 13: Cardiac impression; 14: Basal border; 15: Vertebral part; 16: Aortic impression; 17: Esophageal impression; 18: Groove for caudal vena cava.
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Figure 6-29. Bifurcation of trachea. A) Horizontal histological section of lungs. Hematoxylin-eosin stain (10X). B) Detail of bifurcation. PAS-alcian blue stain (40X). C) Magnification of carina tracheae. Hematoxylin-eosin stain (200X). 1: Left lung; 2: Cranial lobe (right lung); 3: Middle lobe (right lung); 4: Caudal lobe (right lung); 5: Root of lung (structures that enter the lung at the hilus); 6: Trachea; 7: Left main bronchus; 8: Right main bronchus; 9: Carina tracheae; 10: Left pulmonary vein; 11: Pulmonary vein of cranial lobe; 12: Pulmonary vein of middle lobe; 13: Left cranial vena cava; 14: Tracheobronchial lymph node; 15: Pulmonary lymph node; 16: Esophagus.
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Figure 6-31. Respiratory part (gas exchange area). A) Distal airways and alveoli. Scanning electron microscopy image. Araldit® airway cast (Bar = 250 μm). B) Histological section. Hematoxylin-eosin stain (200X). C) Structure of alveolus. Semithin section. Toluidin blue stain (1,000X). D and E) Type I and type II pneumocytes, respectively. Transmission electron microscopy images (15,000X and 10,000X, respectively). 1: Terminal bronchiole; 2: Alveolar duct; 3: Alveolar sac; 4: Pulmonary alveolus; 5: Clara cell; 6: Pneumocyte type I (squamous alveolar epithelial cell); 7: Pneumocyte type II (granular alveolar epithelial cell); 8: Capillary; 9: Nucleus; 10: Cytoplasm of pneumocyte type I; 11: Cytoplasm of endothelial cell; 12: Basement membrane; 13: Lamellar body; 14: Microvilli.
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Figure 6-32. Relationship between lungs and main thoracic vascular trunks. A and B) Transverse sections of thorax. Section and corresponding magnetic resonance image at level of vertebra T7. Cranial view. C) Arterial injection with green latex. Alizarin red stained and clearing. Caudal view of thorax section. 1: Right lung; 2: Left lung; 3: Spinal cord; 4: Vertebral body; 5: Vertebral arch; 6: Epaxial muscles; 7: Sternum; 8: M. pectoralis profundus; 9: Right ventricle; 10: Left ventricle; 11: Right atrium; 12: Left atrium; 13: Esophagus (thoracic part); 14: Thoracic aorta; 15: Right pulmonary vein; 16: Left pulmonary vein; 17: Caudal vena cava; 18: Dorsal intercostal arteries; 19: Coronary arteries.
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Figure 6-33. Distribution of intrapulmonary bronchi, arteries and veins. Left lung. A) Broncography. B) Arteriography. C) Histological section. Mallory’s trichrome stain (40X). 1: Left main bronchus; 2: Segmental bronchi; 3: Bronchioli; 4: Terminal bronchioli and alveolar ducts; 5: Left pulmonary artery; 6: Segmental arteries; 7: Bronchial rami; 8: Segmental veins; 9: Left pulmonary vein.
The respiratory apparatus is formed by two major functional parts, respiratory tracts or airways, which are responsible for conducting the air, and the respiratory part, where gasses are exchanged, principally the release of carbon dioxide and the uptake of oxygen. For the anatomical description, we will use the human classical terms «upper» respiratory tract and «lower» respiratory tract. The upper respiratory tract includes the organs located within the skull, that are, nasal cavities, paranasal sinuses and nasopharynx, whereas the lower respiratory tract consists of the larynx, trachea and lungs. The airways are responsible not only for conducting the air, but also for conditioning the temperature and moisture of the inspired air, as well as removing impurities. In addition, the airways have important functions such as olfaction and phonation, and they are related with sexual behavior.
■ ■ NASAL CAVITY There are two nasal cavities or nasal fossas, which are symmetrical and separated by the nasal septum. The openings of these cavities are the nasal orifices, also known as nares or nostrils, which are located at the tip or apex of the nose. The external nose is supported only by cartilage and covered by a modified skin called the nasal plate (Fig. 6-1). The nasal cavities are bounded by the nasal bones, the incisive bones and the maxillae. The cribriform plate of the ethmoid bone and the choanae, the bone orifices which communicate with the nasopharynx, are the caudal limit of nasal cavities. The nasal septum consists of a bony part (the perpendicular plate of the ethmoid bone and the vomer) and a cartilaginous part (the cartilage of the nasal septum) lying on the vomer. In addition, on its rostral part, the mouse also has a membranous part (Fig. 6-3) that facilitates the mobility of the external nose. In mice the nasal septum is not complete because, just before entering into the nasopharynx, it presents a small communication between both nasal fossas which is referred to as the window of the nasal septum (Fig. 6-16). This window has also been described in rats, hamsters and guinea pigs, and in nasal instillation experiments with these species, each nasal cavity cannot be treated individually. At this level, the mouse has focal aggregates of nasal-associated lymphoid tissue (NALT). Because of their strategic position at the entrance of nasopharyn-
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geal meatus, these mucosal lymphoid aggregates have an important role in regional immune response. NALT has been considered to be the homolog of the human tonsil. The nasal cavity is structurally and functionally a complex. In its interior the nasal cavity has the conchae, which are spiral bone laminas coated with mucosa. The mouse has two nasal conchae, the dorsal nasal concha and the ventral nasal concha, which are analogues of the superior and inferior nasal conchae of man, as well as the ethmoid conchae which are known as ethmoturbinates (Fig. 6-3). In mice, the dorsal nasal concha is part of the nasal bone, while the ventral nasal concha is part of the incisive bone, which is different from what is seen in most animal species (Fig. 6-4). The ethmoturbinates are delicate osseous scrolls of the ethmoid bone in the caudal part of the nasal cavity, and because of their complex structure they are also called collectively as the ethmoidal labyrinth (Figs. 6-2 and 6-3). The mouse has four major ethmoid conchae, also known as endoturbinates (I-IV), which extend far into the nasal cavity, and a series of smaller and more superfi cial conchae denominated as ectoturbinates located between them (Figs. 6-3, 6-14 and 6-17). The spaces between the conchae are called meatuses. The dorsal nasal meatus is the space located dorsally to the dorsal nasal concha. The ventral nasal meatus is the space between the ventral nasal concha and the floor of the nasal cavity and is the only one that communicates caudally with the nasopharynx via the nasopharyngeal meatus. The space between the dorsal and ventral nasal conchae is the middle nasal meatus whereas the common nasal meatus is the name given to the space between the nasal septum and conchae. Finally, the spaces between the ethmoturbinates are called the ethmoidal meatuses (Figs. 6-4 and 6-13). The entire nasal cavity is lined by different kinds of epithelia which determine three different regions. The ventral part of the vestibule or entrance of the nasal cavity is the cutaneous region lined by a squamous epithelium similar to the epithelium of the external nose. It is a stratified epithelium composed of basal cells and several layers of squamous cells that become progressively more flattened towards the surface (Fig. 6-5). The nasal conchae, and most of the nasal septum and the walls of the nasal cavity are lined with respiratory epithelium and therefore collectively they are referred as the respiratory region. The
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typical respiratory epithelium is a pseudostratified ciliated columnar epithelium, more or less columnar depending on the area, composed by ciliated, non-ciliated and basal cells. In mice, the typical respiratory epithelium can be found lining the medial part of the nasal conchae and the central part of the nasal septum (Fig. 6-6). In some areas, especially in the ventral part of the nasal septum, the respiratory epithelium has numerous goblet cells which produce mucin (Fig. 6-7). In humans, there is a gradual rostrocaudal increase in the number of goblet cells in the nasal cavity. In other areas of the nasal cavity, the mouse presented the transitional respiratory epithelium. This type of epithelium is lining the lateral part of the nasal conchae and in the lateral part of the nasal meatuses. This epithelium is composed of cuboidal ciliated cells and interspersed cuboidal non-ciliated cells (Fig. 6-8). Below the respiratory epithelium is found the lamina propria formed by collagen cells, blood vessels, nerves, nasal glands and a well-developed nasal cavernous plexus. This venous cavernous plexus expands or contracts depending on temperature, humidity and carbon dioxide concentration in the inspired air. Summarizing, the respiratory mucosa is responsible for conditioning the inspired air, it removes impurities through the cilia, it humidifi es air by evaporation of mucus, and it heats air through heat exchange with the blood of the cavernous plexus. These functions are particularly important in animals like mice because all the inspired air enters through the nasal cavity. To complete the nasal cavity epithelial lining there is an olfactory region located caudally. In the mouse, the ethmoturbinates and dorsal nasal meatus are covered by olfactory epithelium. This epithelium is similar to humans and consists of sustentacular cells, which are columnar secretory cells with microvilli, neurosensory olfactory cells arranged in five or six layers, and basal cells (Fig. 6-15 and 13-39). The olfactory neurosensory cells are bipolar neurons with dendritic process that terminate as olfactory vesicle in the apical part of the epithelium. These olfactory vesicles have several radiate non-motile cilia that are receptive for different varieties of scents. The axon of olfactory neurosensory cells extends towards the basal part of the epithelium to form unmyelinated nerves, the olfactory nerves, which make synapses with neurons in the olfactory bulb. In addition to these nerves, blood vessels and the olfactory glands, or Bowman’s glands, can also be found in the lamina propria of the olfactory mucosa (Fig. 6-15 and 13-39). The olfactory glands are simple tubule-alveolar glands whose secretion moistens the mucosa and acts as a solvent for olfactory stimuli. The ratio of the three types of epithelium in mice is approximately 7 % squamous epithelium, 46 % respiratory epithelium and 47 % olfactory epithelium, but can vary with age and mouse strain. The proportion of olfactory epithelium in mice is much higher than in man (about 3 %). The nasal epithelium is susceptible to injury, especially from inhaled toxics. For routine examination in toxicological or carcinogenic studies, standardized cross
sections of the nasal cavity in at least three levels should be analyzed. Level 1 is a transverse section made caudally to the superior incisor teeth (Fig. 6-4), level 2 a transverse section made caudally to the incisive papilla (Fig. 6-13) and level 3 a transverse section made through the second superior molar tooth (Fig. 6-14). The nasolacrimal duct can be observed in the rostral sections of the nasal cavity. This duct originates within the lacrimal sac, at the medial angle of the eye. From there, the most caudal part of the nasolacrimal duct is located laterally to the root of the incisor tooth (Fig. 6-13), it then runs along the ventral part of the tooth (Fig. 6-12) and finishes in a medial position in relation to the tooth (Fig. 6-4), where it empties ventromedially to the nasal cavity. The mouse nasolacrimal duct has a large diameter, is lined by stratifi ed squamous epithelium and is surrounded by the nasal cavernous plexus, which is especially developed in the caudal part of the duct (Fig. 6-13). The mouse has a well-developed vomeronasal organ (Jacobson’s organ) located in the rostral part of the nasal cavity. This organ is composed of two caudally blindended epithelial tubes, the vomeronasal ducts which open into the nasal vestibule through a narrow duct. The vomeronasal organ is located on either side of the nasal septum. In most species, this organ is enclosed by a cartilaginous capsule. However, in mice it present a osseous capsule, the vomeronasal bone, is a dilatation of the rostral part of the vomer (Fig. 6-9). The vomeronasal duct is lined by two types of epithelium (Fig. 6-10). Its medial wall is lined with a crescent-shaped sensory epithelium that is similar to the olfactory epithelium. However, its bipolar neurons, are without cilia and the sustentacular cells have an oval nuclei. From this sensory epithelium emerges the vomeronasal nerve which will form synapses in the accessory olfactory bulb. The lateral wall of the vomeronasal duct is formed by a non-sensory ciliated columnar epithelium. A large blood vessel runs laterally to the vomeronasal duct (Figs. 6-10 and 6-11). Changes in blood flow within this vessel influence the arrival of stimuli to the vomeronasal organ. This organ is able to collect non-volatile odoriferous stimuli (pheromones) from biological fluids such as urine, skin secretions or saliva. Pheromones play a crucial role in both reproductive physiology and sexual behavior. The vomeronasal organ forms part of the accessory olfactory system. In humans, the vomeronasal organ is a vestigial organ and, although it has been described in both development and adulthood, its functionality is far from clear. Located ventrally to the vomeronasal organ are the incisive ducts which are a communication between nasal and oral cavities (Fig. 6-12). These ducts are lined by stratified squamous epithelium as a continuation of the nasal vestibule epithelium. They originate independently from the two nasal fossas and open in two orifices located laterally in the incisive papilla of hard palate. Unlike other animal species and man, the mouse only has a single paranasal sinus, the maxillary sinus. This sinus is voluminous and mainly located above the zygo-
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matic arch (Fig. 6-16 and 6-17). Its rostrodorsal part communicates with the ethmoid labyrinth. The middle part of the sinus communicates with caudal part of the middle nasal meatus through the nasomaxillary opening. The maxillary sinus ends as a caudal recess at the level of the fi rst upper molar tooth (Fig. 6-17). The epithelium lining the sinus is a typical ciliated respiratory epithelium. Surrounding the maxillary sinus there are two nasal glands; the lateral nasal gland and the maxillary gland. These two glands are mixed glands and morphologically difficult to distinguish although they do show very different affinities for PAS staining (Fig. 6-16). The lateral nasal gland (Steno’s gland) surrounds the rostral and ventrolateral part of the sinus, and empties through a large excretory duct (Fig. 6-4) at the entrance of the nasal cavity. The maxillary gland surrounds the rest of the maxillary sinus, and drains directly into the sinus through small excretory ducts. The mouse has other smaller nasal glands including the anterior glands and the posterior glands of the nasal septum, which are located in the dorsal and ventral part of the septum, respectively. Whereas the anterior glands have the appearance of mucous glands, the posterior glands are of a serous aspect and PAS-positive (Fig. 6-11). The excretory ducts of the anterior glands open into the nasal vestibule. The posterior glands of the nasal septum are partially located within the vomeronasal bone. Because of this, they are also named as vomeronasal glands. These glands empty their secretions into the vomeronasal duct. Two excretory ducts can be seen in the junctions between the sensory and non-sensory epithelium of vomeronasal ducts (Fig. 6-11). The blood supply of mouse nasal cavity comes from different arteries (Fig. 6-18). The major palatine artery passes through the major palatine foramen and sends branches to the hard palate and the rostral region of the nose. The sphenopalatine artery passes through the foramen of the same name to enter and vascularize the nasal cavity. The external ethmoidal artery, a branch of the ophthalmic artery, enters through the ethmoidal foramen to vascularize the ethmoturbinates. All these arteries arise from the maxillary artery. In addition, the internal ethmoidal arteries arrive to the nasal cavity passing through the cribriform plate of the ethmoid bone. The internal ethmoidal arteries, which are branches of the rostral cerebral arteries, supply the most of the nasal conchae and nasal septum, unlike other animal species where the main blood supply for the nasal cavity arrives from the external ethmoidal arteries.
■ ■ LARYNX After passing through the nasal cavity and nasopharynx, inspired air enters the larynx. The larynx is a tubeshaped musculocartilaginous organ whose main function is to let the air pass from the pharynx to the trachea, preventing aspiration of food or any other foreign material into the lower respiratory tract. In addition, the larynx is the organ of phonation.
The mouse larynx, as in all domestic mammals, consists of three unpaired cartilages: the epiglottic cartilage, the thyroid cartilage and the cricoid cartilage, and two arytenoid cartilages (Fig. 6-19). The epiglottic cartilage forms the epiglottis which opens and closes the laryngeal inlet. The thyroid cartilage, is formed by a double lamina in form of a «U» opened dorsally. The thyroid cartilage articulates caudally with the cricoid cartilage, a closed ring-shaped cartilage which is composed of a ventral arch and a dorsal lamina. Within the thyroid cartilage, and articulating caudally with the cricoid cartilage, are located the arytenoid cartilages. They are hook-shaped and their corniculate processes are separated into two little cartilages in humans (corniculate cartilages). The laryngeal inlet is an orifi ce delimits the epiglottis, the corniculate tubercles (corniculate processes covered by mucosa) and the aryepiglottic folds (Fig. 6-22). Upon entering the laryngeal cavity, the vestibule of the larynx is found. There the mouse has an enormous median laryngeal recess (Figs. 6-22 and 6-23). The caudal limit of the vestibule of the larynx are the vocal folds or vocal cords, which are produced by the prominence of vocal muscles. The mouse, unlike humans and other animal species, have no vestibular folds or false vocal cords. The glottis consist of the paired arytenoid cartilages dorsally and the paired vocal folds ventrally. The narrow space left between the vocal folds is the rima glottidis or glottic cleft (Fig. 6-23). As air passes, vibration of the vocal folds occurs and, depending on their degree of contraction, the mouse emits different types of sounds, although most are in an ultrasonic range. Caudal to the glottis the lumen of larynx becomes wider. This short part of the larynx is called the infraglottic cavity, which is continuous with the trachea. The epithelium lining the laryngeal inlet is like the epithelium of the oropharynx, a stratified squamous columnar epithelium. Caudally to this it becomes pseudostratifi ed, and returns to be a ciliated columnar respiratory epithelium in the infraglottic cavity. The areas of transition between the different epithelia, such as between the base of the epiglottis and the median laryngeal recess, are very sensitive to damage from inhaled toxic or irritating agents. In the submucosa of the larynx, the mouse has some well-developed laryngeal glands. They are mixed glands, but with predominance of mucous or serous glands depending on the region. Can be distinguished one epiglottic gland (Fig. 6-22) and several laryngeal glands between the cricoid cartilage and the first tracheal cartilage (Fig. 6-24). In all mammals, a set of bones called the hyoid bone or hyoid apparatus (Figs. 6-20 and 6-21), is responsible for fixing the larynx and tongue to the base of the cranium, articulating with the thyroid cartilage of the larynx and the temporal bone. The mouse hyoid bone is similar to humans and is attached to the larynx and cranium only by ligaments and muscles. It has an unpaired transversal bone, the basihyoid (body), and two paired bones, the ceratohyoids (lesser horns) and the thyrohyoids (greater
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horns). The ceratohyoid is more rostral and highly developed in the mouse, joining with the temporal bone by the stylohyoid ligament. The thyrohyoid binds the thyroid cartilage through the thyrohyoid ligaments.
■ ■ TRACHEA The trachea is a cartilaginous tube formed by a series of tracheal cartilages, joined together by annular ligaments (Figs. 4-13, 4-15 and 6-9). These cartilages give the trachea rigidity and prevent its collapse. In the mouse, the trachea has about 15 cartilages with an approximate internal diameter of 1.5 mm. The C-shaped cartilages are open dorsally. The dorsal space is bridged by connective tissue and the tracheal muscle, a smooth muscle that is responsible for contracting the lumen of the trachea (Fig. 6-24). The trachea extends from the cricoid cartilage of the larynx to its bifurcation into two main bronchi (Fig. 6-27). The trachea is divided into a cervical part situated in the ventral region of the neck, and a thoracic part inside the thorax. The epithelial lining of the trachea is a pseudostratified columnar respiratory epithelium consisting of ciliated and clara cells. The proportion of clara cells is increased in the caudal part of the trachea, and goblet cells are only found rarely. The location of clara cells in the trachea is unique to the mouse since these cells are only found in the caudal part of airways of most species. There are tracheal glands in the submucosa, although they are restricted to the craneal part of the trachea in the mouse (Fig. 6-24).
■ ■ LUNGS The left and right lungs are two elastic organs that occupy most of the thoracic cavity (Figs. 6-25 and 6-26). In the mouse, the total lung capacity is about 1 ml. The left lung of the mouse is smaller and, unlike what happens in other animal species or humans, it is not divided. The right lung has four lobes; cranial, middle, caudal and accessory lobes (Figs. 6-25 to 6-29). Each lung has a costal surface, in contact with the thoracic wall; a medial surface, which contacts the vertebrae and mediastinum; and a diaphragmatic surface on the caudal portion of the lung in contact with the diaphragm. In addition, the right lung has interlobular surfaces between the different lobes. On the medial surface is the hilus of the lung, which is the area where the bronchi, vessels and nerves enter and leave the lung. The collective name for these structures is the root of the lung (Fig. 6-29). In the hilus of the lung, the visceral pleura that covers the lung folds and continues as the parietal pleura, which lines the walls of the thoracic cavity and the mediastinum. The pleural cavity is situated between the visceral and parietal pleurae. There are two independent pleural cavities, one for each lung, containing only a thin film of fluid to reduce friction during respiration. The space between the right and the left pleural cavities is the mediastinum, in which the heart and other thoracic organs, mainly the great vessels, nerves and esophagus are situated.
The bronchial tree begins when the trachea divides into the two left and right main bronchus (Figs. 6-26 to 6-29). In the interior of the bifurcation there is a crest known as the carina tracheae that marks the separation of the two main bronchi. These continue surrounded by bronchial cartilages, which disappears once the bronchus enters in the lungs (Fig. 6-29). Bronchial cartilages is replaced by smooth muscle. Within the lung, the right main bronchus divides into several lobular bronchi, one for each lobe. The lobular bronchi branch further, going in different directions as segmental bronchi (Fig. 6-30) that ventilate the bronchopulmonary segments into which the lung parenchyma is divided. In turn, the segmental bronchi branch into bronchioles, of a similar structure to the last ones, but of smaller diameter and ending in the terminal bronchioles. The mouse has large airways, representing a greater percentage of the total lung volume compared to other species. Usually, the mouse has no respiratory bronchioles and the terminal bronchioles often divide directly into the alveolar ducts (Fig. 6-31). The respiratory epithelium of the bronchial tree is a simple epithelium that is transformed from columnar to cuboidal. The epithelium of the intrapulmonary airways has no basal cells and is formed by ciliated cells, occasional neuroendocrine cells and a large number of secretory cells, the clara cells (Fig. 6-30). Clara cells have an irregular form and the nucleus is situated at the base of the cell with abundant agranular endoplasmic reticulum and numerous electron-lucid secretory granules in the apical cytoplasm. The granules are mainly glycoproteins that help degrade toxins, protect the epithelium and reduce surface tension. In most species, including humans, these cells are only found in the bronchioles. However, in the mouse they can be found from the trachea down, further increasing in the more distal portions, and representing about 60 % of the epithelial cells of the bronchial tree. Other cells like serous cells or brush cells are rare in intrapulmonary bronchi and bronchioles of mice. It is in the respiratory part (gas exchange area) or lung parenchyma (Fig. 6-31) where gas exchange occurs. Here, the terminal bronchioles branch into the alveolar ducts which open into the alveolar sacs. The alveolar sacs are groups of pulmonary alveoli shaped as a bunch of grapes. These alevoli are small in mice (40 - 80 microns) compared to those of other species. The alveoli are supported by interstitial tissue with abundant elastic tissue, collagen and numerous capillaries. The epithelium of the alveolus is composed of two types of pneumocytes. Type I or respiratory pneumocytes are elongated flat cells. Their cytoplasm together with a dual basement membrane and the endothelial cell cytoplasm form the wall of the alveolus (the blood-air barrier) (Fig. 6-31), where gas exchange occurs. Type II or granular pneumocytes are found between the interalveolar septa and contain lamellar bodies that give them the granular appearance. These lamellar bodies produce phospholipid-rich surfactant required to reduce the surface tension in the alveoli. Only Type II
6. Respiratory apparatus
pneumocytes have mitotic capacity and moreover, they also are able to differentiate into type I cells. The main function of the lungs is to oxygenate blood. The blood reaches the lungs via the left and right pulmonary arteries (Fig. 11-22), which will continue branching as does the bronchial tree, down into the capillaries which are tightly related to the alveoli of the lung. However, in the mouse the segmental arteries do not accompany the segmental bronchi, but instead run between the bronchopulmonary segments (Fig. 6-33). This situation is opposite to that which occurs in man, where the segmental arteries accompany the segmental bronchi. The blood, once oxygenated, returns through the pulmonary veins (Fig. 11-22) to the heart following the same pattern of branching and
accompanying the bronchial tree (Fig. 6-33). In addition to this pulmonary circulation (functional), there is a bronchial circulation (nutritional) that comes from branches from the thoracic aorta and the intercostal arteries. In the mouse, there is controversy about whether this vascularization reaches the alveolar level as in other species, or if it only nourishes the trachea and the main bronchi without penetrating into the lung parenchyma. With respect to the lymph nodes, the mouse has only one right tracheobronchial lymph node, located cranially to the origin of the right main bronchus and it may have small pulmonary lymph nodes within the lung parenchyma (Fig. 6-29). Bronchiole associated lymphoid tissue (BALT) is rarely observed in the lungs of healthy mice.
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Figure 6-5. Stratified squamous epithelium. A) Hematoxylin-eosin stain (1,000X). B) Staining with Lycopersicon esculentum lectin revealed by DAB (brown) and hematoxylin (1,000X). 1: Squamous cells; 2: Basal cells; 3: Lamina propria.
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Figure 6-10. Structure of vomeronasal organ. Transverse sections. A) Histological section. Hematoxylin-eosin stain (100X). B) Magnetic resonance image of nasal cavity (level 1). C) Ultrasound image. D) Staining with Lycopersicon sculentum lectin revealed by DAB (brown) and hematoxylin (100X). E and F) Magnifications of sensory and non-sensory epithelia, respectively (1,000X). 1: Vomeronasal bone (vomer); 2: Sensory epithelium; 3: Non-sensory epithelium; 4: Vomeronasal duct; 5: Blood vessel of vomeronasal organ; 6: Lamina basal; 7: Capillary; 8: Vomeronasal nerve; 9: Posterior gland of nasal septum; 10: Cartilage of nasal septum; 11: Respiratory epithelium; 12: Nasal cavernous plexus; 13: Ventral nasal meatus; 14: Nasal bone; 15: Skin; 16: Dorsal nasal concha; 17: Ventral nasal concha; 18: Nasolacrimal duct; 19: Root (dental pulp) of upper incisor tooth; 20: Neurosensory olfactory cells; 21: Sustentacular cell; 22: Ciliated columnar cell; 23: Basal cells.
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Figure 6-11. Glands of nasal septum. Transverse histological section (100X) and magnifications stained with hematoxylin-eosin (400X). A) PAS stain. B) Anterior gland of nasal septum. C and D) Posterior gland of nasal septum. 1: Anterior gland of nasal septum; 2: Posterior gland of nasal septum; 3: Gland of vomeronasal organ (posterior gland of nasal septum); 4: Cartilage of nasal septum; 5: Vomeronasal bone (vomer); 6: Vomeronasal duct; 7: Vomeronasal nerve; 8: Blood vessel of vomeronasal organ; 9: Nasal cavernous plexus; 10: Respiratory epithelium; 11: Excretory duct.
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Figure 6-12. Incisive duct. A and B) Incisive papilla. Ventral view of palate and scanning electron microscopy image. C) Transverse histological section of nasal cavity at level of incisive papilla. Hematoxylin-eosin stain (40X). D) Computed tomography image. Transverse section. 1: Incisive papilla; 2: Incisive duct; 3: Orifice of incisive duct; 4: Palatine ridge; 5: Cartilage of nasal septum; 6: Vomeronasal organ; 7: Vomeronasal bone (vomer); 8: Incisive bone; 9: Root of upper incisor tooth; 10: Nasolacrimal duct; 11: Dorsal nasal concha; 12: Ventral nasal concha; 13: Dorsal nasal meatus; 14: Ventral nasal meatus.
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Figure 6-13. Transverse section of nasal cavity. Level 2. A) Masson’s trichrome stain (20X). B) Computed tomography image. C) Detail of nasolacrimal duct epithelium. Hematoxylin-eosin stain (1,000X). 1: Nasal bone; 2: Incisive bone; 3: Cartilage of nasal septum; 4: Vomer; 5: Vomeronasal bone (vomer); 6: Blood vessel of vomeronasal organ; 7: Nasal cavernous plexus; 8: Dorsal nasal concha; 9: Ventral nasal concha; 10: Root of upper incisor tooth; 11: Dental alveolus of upper incisor tooth; 12: Nasolacrimal duct; 13: Dorsal nasal meatus; 14: Common nasal meatus; 15: Ventral nasal meatus; 16: Olfactory epithelium; 17: Palatine fissure; 18: Palatine mucosa; 19: Oral cavity; 20: Squamous cells; 21: Basal cell; 22: Lamina propria.
6. Respiratory apparatus
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Figure 6-14. Transverse section of nasal cavities. Level 3. A) Masson’s trichrome stain (20X). B) Computed tomography image. 1: Frontal bone; 2: Second upper molar tooth; 3: Maxilla; 4: Perpendicular plate (ethmoidal bone); 5: Nasopharyngeal meatus; 6: Nasal associated lymphoid tissue (NALT); 7: Hard palate; 8: Palatine mucosa; 9: Palatine raphe; 10: Major palatine artery (inside major palatine canal); 11: Ectoturbinates; 12: Endoturbinate III; 13: Endoturbinate IV; 14: Olfactory bulb; 15: Olfactory nerves; 16: Lacrimal gland of third eyelid (Harderian gland).
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Figure 6-15. Olfactory epithelium. Histological sections (1,000X). A) Hematoxylin-eosin stain. B) Masson’s trichrome stain. C) Staining with Lycopersicon sculentum lectin revealed by DAB (brown) and hematoxylin. D) PAS and Harris’s hematoxylin stain. 1: Sustentacular cells; 2: Neurosensory olfactory cells; 3: Basal cell; 4: Basal lamina; 5: Blood vessels; 6: Olfactory nerves; 7: Olfactory (or Bowman’s) glands; 8: Excretory duct of olfactory gland; 9: Olfactory vesicles.
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Figure 6-16. Window of nasal septum and maxillary sinus. Transverse sections of nasal cavity, rostrally to level 3. A) Computed tomography image. B) Glands surrounding maxillary sinus. PAS stain (40X and 400X, respectively). C) Window of nasal septum. Hematoxylin-eosin stain (40X). 1: Window of nasal septum; 2: Maxillary sinus; 3: Maxillary gland; 4: Lateral nasal gland; 5: Respiratory epithelium; 6: Nasal associated lymphoid tissue (NALT); 7: Frontal bone; 8: Zygomatic process (maxilla); 9: Vomer; 10: Palatine process (maxilla); 11: Ectoturbinate; 12: Endoturbinate III; 13: Endoturbinate IV; 14: Basal lamina (floor of ethmoidal labyrinth); 15: Cartilage of nasal septum; 16: Palatine fissure; 17: Major palatine artery; 18: Palatine mucosa.
6. Respiratory apparatus
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Figure 6-17. Maxillary sinus. Computed tomography images (A-E) and magnetic resonance images (F and G). A) Sagittal section of nasal cavity indicating planes of transverse sections. B) Communication with ethmoidal labyrinth. C) Communication with nasal cavity. D) Maxillary sinus at level of zygomatic process. E) Caudal recess of maxillary sinus. F) Sagittal section of nasal cavity showing reference of transverse section. G) Maxillary sinus at level of zygomatic process.
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Figure 6-18. Arterial vascularization of nasal cavity. A) Arterial injection with Araldit® (red). Soft tissue was macerated with pancreatin. Nasal bone, incisive bone, maxilla and mandible of left side were removed. B) Arterial injection with latex (green). Alizarin red stained and clearing. Horizontal section. 1: Nasal bone; 2: Incisive bone; 3: Mandible; 4: Maxilla; 5: Frontal bone; 6: Cribriform plate (ethmoidal bone); 7: Eyeball; 8: Lacrimal gland of third eyelid (Harderian gland).; 9: Dorsal nasal concha; 10: Ventral nasal concha; 11: Ethmoturbinates; 12: Vomeronasal bone; 13: Ethmoidal foramen; 14: Sphenopalatine foramen (opened); 15: Maxillary artery (through alar canal); 16: Ophtalmic artery; 17: Infraorbital artery; 18: Sphenopalatine artery; 19: Major palatine artery; 20: Septal nasal artery; 21: External ethmoidal artery; 22: Ethmoidal branch; 23: Internal ethmoidal arteries; 24: Caudal lateral nasal artery; 25: Caudal septal nasal artery.
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Figure 6-19. Topography of larynx and laryngeal cartilages. A) Median section of head. B) Magnetic resonance image. C) Ventral view of neck. M. sternohyoideus and salivary glands were removed. D) Ventral view of laryngeal cartilages. E) Dorsal view of laryngeal cartilages. 1: Nasal cavity; 2: Brain; 3: Spinal cord; 4: Tongue; 5: Hard palate; 6: Soft palate; 7: Nasopharynx; 8: Oropharynx; 9: Basihyoid; 10: Larynx; 11: Trachea; 12: M. sternohyoideus; 13: M. masseter; 14: M. mylohyoideus; 15: M. sternomastoideus; 16: M. pectoralis superfi cialis; 17: External acoustic meatus; 18: Thyroid gland; 19: Cricothyroid ligament; 20: Anular ligament; 21: Tracheal cartilage; 22: Epiglottic cartilage; 23: Thyroid cartilage; 24: Arytenoid cartilages; 25: Cricoid cartilage; 26: Left lamina (thyroid cartilage); 27: Right lamina (thyroid cartilage); 28: Laryngeal prominence; 29: Caudal thyroid notch; 30: Caudal horn (thyroid cartilage); 31: Cricothyroid joint; 32: Corniculate process (arytenoid cartilage); 33: Arch of cricoid cartilage; 34: Lamina of cricoid cartilage.
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6. Respiratory apparatus
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Figure 6-21. Hyoid bone (hyoid apparatus). Topography and structure. A) Computed tomography image. Transverse section. B) Transverse histological section and magnification of ceratohyoid. Hematoxylin-eosin stain (10X and 100X, respectively). C) Scanning electron microscopy image. Caudal view. 1: Basihyoid (body of hyoid bone); 2: Ceratohyoid (lesser horn); 3: Thyrohyoid (greater horn); 4: Middle ear; 5: Internal ear; 6: Oropharynx; 7: Nasopharynx; 8: Soft palate; 9: Pharyngeal glands; 10: External carotid artery.
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Figure 6-22. Laryngeal inlet. A) Rostral view of laryngeal inlet. B) Laryngeal cavity dorsally opened. Scanning electron microscopy image. C) Transverse histological section. Hematoxylin-eosin stain (40X). 1: Epiglottis (laryngeal surface); 2: Apex (epiglottis); 3: Lateral borders (epiglottis); 4: Aryepiglottic fold; 5: Corniculate tubercle; 6: Root of tongue; 7: Lateral glossoepiglottic fold; 8: Piriform recess; 9: Soft palate (sectioned); 10: Esophagus (opened); 11: Median laryngeal recess; 12: Vocal fold; 13: Laryngopharynx; 14: Epiglottic cartilage; 15: Thyroid cartilage; 16: M. sternohyoideus; 17: Pharyngeal glands; 18: Epiglottic gland.
6. Respiratory apparatus
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Figure 6-24. Topography and structure of trachea. A and B) Transverse histological sections. Hematoxylin-eosin stain (40X). C) Ultrasound image of trachea. Sagittal section. D) Respiratory epithelium of trachea. Hematoxylin-eosin stain (1,000X). 1: Lamina of cricoid cartilage; 2: Arch of cricoid cartilage; 3: Tracheal cartilage; 4: Esophagus; 5: M. cricoarytenoideus dorsalis; 6: Thyroid gland; 7: M. trachealis; 8: Laryngeal gland; 9: Tracheal gland; 10: Mandibular gland; 11: M. sternohyoideus; 12: Ciliated columnar cell; 13: Clara cell; 14: Basal cells; 15: Lamina propria.
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Figure 6-25. Topography of lungs. A) Computed tomography image. 3D reconstruction. Left lateral view. B) Laterolateral broncography. C) Lateral view of left lung. Left thoracic limb and muscles of thoracic wall were removed. 1: Trachea; 2: Lung; 3: First rib; 4: Eighth rib; 5: Sternum; 6: Axis; 7: Pleural cupula; 8: Mm. intercostales (partially removed); 9: Epaxial muscles; 10: M. pectoralis profundus; 11: M. rectus abdominis.
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Figure 6-26. Topography of lungs. A) Computed tomography image. 3D reconstruction. Dorsal view. B) Thoracic cavity dorsally opened. C) Dorsoventral broncography. D) Magnetic resonance image. Horizontal Section. 1: Left lung; 2: Right lung; 3: Cranial lobe (right lung); 4: Middle lobe (right lung); 5: Caudal lobe (right lung); 6: Accessory lobe (right lung); 7: Diaphragm; 8: Esophagus (thoracic part); 9: Thoracic aorta; 10: Trachea; 11: Left main bronchus; 12: Right main bronchus; 13: Left pulmonary artery and vein; 14: Caudal vena cava; 15: Cranial lobar bronchus; 16: Liver; 17: Stomach.
6. Respiratory apparatus
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Figure 6-27. Lobes of lungs. Araldit® airway cast. A) Dorsal view. B) Ventral view. C) Caudal view (diaphragmatic surface). 1: Left lung; 2: Cranial lobe (right lung); 3: Middle lobe (right lung); 4: Caudal lobe (right lung); 5: Accessory lobe (right lung); 6: Trachea; 7: Left main bronchus; 8: Right main bronchus; 9: Apex of lung; 10: Cranial interlobular fissure; 11: Caudal interlobular fissure; 12: Hilus of lung; 13: Cardiac impression; 14: Basal border; 15: Vertebral part; 16: Aortic impression; 17: Esophageal impression; 18: Groove for caudal vena cava.
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Figure 6-28. Bronchial tree. Araldit® airway cast. A and B) Right lung (ventral view) and left lung (medial view). C and D) Bronchial tree into right lung (medial view) and left lung (ventral view), respectively. 1: Left lung; 2: Cranial lobe (right lung); 3: Middle lobe (right lung); 4: Caudal lobe (right lung); 5: Accessory lobe (right lung); 6: Dorsal border; 7: Ventral border; 8: Basal border; 9: Hilus of lung; 10: Aortic impression; 11: Trachea; 12: Left main bronchus; 13: Right main bronchus; 14: Cranial lobar bronchus; 15: Middle lobar bronchus; 16: Caudal lobar bronchus; 17: Accessory lobar bronchus; 18: Segmental bronchi; 19: Bronchioli.
6. Respiratory apparatus
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Figure 6-29. Bifurcation of trachea. A) Horizontal histological section of lungs. Hematoxylin-eosin stain (10X). B) Detail of bifurcation. PAS-alcian blue stain (40X). C) Magnification of carina tracheae. Hematoxylin-eosin stain (200X). 1: Left lung; 2: Cranial lobe (right lung); 3: Middle lobe (right lung); 4: Caudal lobe (right lung); 5: Root of lung (structures that enter the lung at the hilus); 6: Trachea; 7: Left main bronchus; 8: Right main bronchus; 9: Carina tracheae; 10: Left pulmonary vein; 11: Pulmonary vein of cranial lobe; 12: Pulmonary vein of middle lobe; 13: Left cranial vena cava; 14: Tracheobronchial lymph node; 15: Pulmonary lymph node; 16: Esophagus.
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Figure 6-31. Respiratory part (gas exchange area). A) Distal airways and alveoli. Scanning electron microscopy image. Araldit® airway cast (Bar = 250 μm). B) Histological section. Hematoxylin-eosin stain (200X). C) Structure of alveolus. Semithin section. Toluidin blue stain (1,000X). D and E) Type I and type II pneumocytes, respectively. Transmission electron microscopy images (15,000X and 10,000X, respectively). 1: Terminal bronchiole; 2: Alveolar duct; 3: Alveolar sac; 4: Pulmonary alveolus; 5: Clara cell; 6: Pneumocyte type I (squamous alveolar epithelial cell); 7: Pneumocyte type II (granular alveolar epithelial cell); 8: Capillary; 9: Nucleus; 10: Cytoplasm of pneumocyte type I; 11: Cytoplasm of endothelial cell; 12: Basement membrane; 13: Lamellar body; 14: Microvilli.
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Figure 6-32. Relationship between lungs and main thoracic vascular trunks. A and B) Transverse sections of thorax. Section and corresponding magnetic resonance image at level of vertebra T7. Cranial view. C) Arterial injection with green latex. Alizarin red stained and clearing. Caudal view of thorax section. 1: Right lung; 2: Left lung; 3: Spinal cord; 4: Vertebral body; 5: Vertebral arch; 6: Epaxial muscles; 7: Sternum; 8: M. pectoralis profundus; 9: Right ventricle; 10: Left ventricle; 11: Right atrium; 12: Left atrium; 13: Esophagus (thoracic part); 14: Thoracic aorta; 15: Right pulmonary vein; 16: Left pulmonary vein; 17: Caudal vena cava; 18: Dorsal intercostal arteries; 19: Coronary arteries.
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Figure 6-33. Distribution of intrapulmonary bronchi, arteries and veins. Left lung. A) Broncography. B) Arteriography. C) Histological section. Mallory’s trichrome stain (40X). 1: Left main bronchus; 2: Segmental bronchi; 3: Bronchioli; 4: Terminal bronchioli and alveolar ducts; 5: Left pulmonary artery; 6: Segmental arteries; 7: Bronchial rami; 8: Segmental veins; 9: Left pulmonary vein.