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SYMPOSIUM Architecture of the Lung Morphology and Function Harumi Itoh, MD, PhD,* Mizuki Nishino, MD,† and Hiroto Hatabu, MD, PhD† Abstract: The architecture of the lung is discussed with special focus on lung parenchyma. The lung parenchyma is mainly comprised of numerous air-containing passages and intervening fine structures, corresponding to alveolar ductal lumens and alveoli, as well as alveolar septa and small pulmonary vessels occupying 10% of total parenchymal volume. The shapes and relative arrangements of alveolar ducts and alveoli are discussed in detail, which is followed by a brief description of bronchial circulation and pulmonary lymphatics. (J Thorac Imaging 2004;19:221–227) T he purpose of this article is to demonstrate the architecture of the lung with special focus on lung parenchyma. The term “architecture” simply describes the notion of morphologic and functional correlation.1,2 There are two kinds of lung structures, parenchymal and non-parenchymal structures. The lung parenchyma resembles a sponge, and occupies 90% of total lung volume. Non-parenchymal structures consist of the bronchial tree, pulmonary vessels, and interlobular septa (Fig. 1). As shown in Figure 1B, the bronchi and pulmonary arteries run together, alternated by pulmonary veins. LUNG PARENCHYMA A closer look at the lung parenchyma reveals numerous air-containing passages and intervening fine structures. Both are distributed evenly as seen in the 0.5 mm thick lung slice shown in Figure 2. The passage and intervening structures correspond to alveolar ductal lumens and alveoli, respectively. Alveolar septa and small pulmonary vessels occupy 10% of the total parenchymal volume, that is, the mean density of lung parenchyma is 0.1g/ml, which corresponds to −900HU of CT attenuation.3 ALVEOLAR DUCT AND ALVEOLI An alveolar duct is best viewed in the short axis diameter. Seven or 8 alveoli surround the alveolar ductal lumen. From the *Department of Radiology, University of Fukui Faculty of Medical Sciences, Matsuoka-cho, Yoshida-gun, Fukui, Japan; and †Department of Radiology, Beth Israel Deaconess Medical Center, Boston, MA. Reprints: Hiroto Hatabu MD, PhD, Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Ave., Boston, MA 02215 (e-mail: [email protected]). Copyright © 2004 by Lippincott Williams & Wilkins J Thorac Imaging • Volume 19, Number 4, October 2004 The interalveolar septum is a thin membrane, and the overall shape of the alveolus is polyhedral (Fig. 3A). When we look at the alveolar duct on histology, every alveolar septal membrane appears as a line (Fig. 3B). The 2-dimensional histologic image shown in Figure 3B is more frequently referenced than the 3-dimensional view shown in Figure 3A, which leads to a lack of 3-dimensional understanding of lung parenchyma. It is possible to distinguish alveolar ductal lumen, alveolar entrance, lateral wall of alveolus, and dome of alveolus on both Figures 3A and 3B. The diameter of the ductal lumen is 0.3 mm, and the mean size of the alveolus is 0.2 mm. The alveolar duct length is about 1 mm in the long axis. The inner surface of the alveolar duct is covered by a sheet of alveoli. The shape of each alveolar entrance is not round but polygonal, like a honeycomb. At higher magnification, a small hole in the alveolar dome can be seen, which is Kohn pore (Fig. 4). The photographs of a real honeycomb show the entrance of each cell as hexagonal in shape (Fig. 5). Mathematically, the overall shape is ideal for maximum cell volume in a limited space. The honeycomb structure is composed of a single layer of alveoli but in the lung parenchyma, the alveoli walls are double-layered. When we look at a model of a honeycomb (Fig. 6A), each cell is derived from a rhombic dodecahedron originally described by the German astronomer, Johannes Kepler. Note the imaginary alveolar entrance, lateral wall, and alveolar dome. Each dome is composed of 3 planes. The important geometric feature of this honeycomb model is that exactly the same sheet of cells can be formed on the other side holding the dome in common. The red line in each dome indicates where the lateral wall stands and extends toward the other side. When we compare the model with the magnified view of the alveoli, white lines corresponding to our red lines are seen in the dome of alveoli (Fig. 6B). A double-layered alveolar sheet can be demonstrated in a lateral view, as shown in Figure 7A. Every lateral wall of the alveolus joins to the apex of the alveolar dome. On histology, it is emphasized that the double-layered alveolar sheets hold alveolar domes in common (Fig. 7B). This common histologic image defines the 2-dimensional architectural unit of lung parenchyma. Now we take a histologic look at the architectural unit forming a network in the parenchymal space and sur- 221 Itoh et al J Thorac Imaging • Volume 19, Number 4, October 2004 branching is different from that of a bronchiole, as there is no spur. Next, we discuss the overall shape of the alveolar duct. In Figure 9A, the contact radiograph shows alveolar ducts coated with barium sulfate demonstrating a round radiolucent area, which corresponds to alveolar ductal lumen, as compared with the magnified view of the lung specimen. The lumen is surrounded by polygonal alveoli. Note the characteristic zigzag shaped domes of alveoli and that the overall shape of the alveolar duct is polygonal. The contact radiograph shows the overall shape of the similarly sized bronchiole and alveolar ducts (Fig. 9B). The bronchiole is cylindrical in shape, but the alveolar duct is polygonal. This implies that the alveolar duct has an ideal overall shape for peak lung function. In fact, the histologic image shows the number of alveolar ducts is much greater than that of the bronchioles (Fig. 9C). RESPIRATORY BRONCHIOLE The respiratory bronchiole is called the transitional zone because part of the bronchiolar wall is replaced by alveoli. The number of alveoli increases as the respiratory bronchioles branch out (Fig. 10A). The distance from the respiratory bronchiole to the nearest septal structures of the secondary lobule is constant. For example, in the case shown in Figure 10B, the respiratory bronchiole is separated from the pulmonary vein by lung parenchyma. The distance between the two is maintained at 2 mm. On histologic examination of the respiratory bronchiole, the bronchiolar wall, which is remote from the pulmonary artery, is replaced by a sheet of alveoli (Fig. 10C). A close-up image reveals these alveoli form a double sheet of alveoli where they abut the recurrent branch of the alveolar duct (Fig. 10D). ALVEOLAR CAPILLARY BEDS AND VENULES FIGURE 1. A, Inflated and fixed lung specimens show bronchial tree, pulmonary vessels, and interlobular septa, which are known as non-parenchymal structures. Lung parenchyma occupies 90% of total lung volume. B, A schematic drawing of the lung based on a contact radiograph of the specimen is shown. Note that pulmonary artery and vein run alternatively in the lung. rounding the alveolar ductal lumen (Fig. 8A). Every alveolar duct appears isolated in this image. However, on a 3-dimensional photograph of the lung specimen, the alveolar ducts are characterized by frequent branching (Fig. 8B). The pattern of 222 The important structural component of the interalveolar septum is the alveolar capillary. The capillary beds are calculated to comprise 50% of the volume of alveolar septum, as demonstrated in Figure 11A. The alveolar capillary is a dense network consisting of a number of irregular polygons. According to Weibel, 10% of alveoli come into contact with nonparenchymal structures, such as pulmonary vessels.4 A number of alveoli abut the pulmonary vein (Figs. 11B and 11C). Such alveoli do not form the usual double-layered sheets of alveoli. The alveolar dome contiguous to the vessel is a singlefaced alveolar wall because gas diffusion does not occur toward the pulmonary vessel. In contrast, the interalveolar septum is a double-faced alveolar wall. Gas exchange is possible in both sides of the double-faced alveolar wall. Alveolar capillaries are connected to post- or pre-capillary small vessels (Fig. 12A). Such small pulmonary vessels occupy part of the limited interstitial space between the alveolar ducts (Fig. 12B). © 2004 Lippincott Williams & Wilkins J Thorac Imaging • Volume 19, Number 4, October 2004 Architecture of the Lung FIGURE 2. A, Details of lung parenchyma consisting of numerous aircontaining passages and intervening fine structures, corresponding to alveolar ducts and alveoli. B, A magnified view of Fig. 2A. FIGURE 3. A, Short axis view of alveolar duct surrounded by 7–8 alveoli. Note a thin membranous interalveolar septum and polyhedronshaped alveolus. B, Histologic image of alveolar duct showing alveolar septal membrane as a line. FIGURE 4. An enlarged view of the alveolar dome shows Kohn pore as small hole (arrow). FIGURE 5. Photograph of a real honeycomb. Note the hexagonal shape of the entrance of each cell. FIGURE 6. A, Model of a honeycomb. Note the exact same sheet of cells formed on the other side holding the dome in common. B, A magnified view of alveoli showing white lines similar to the red lines in the honeycomb model. © 2004 Lippincott Williams & Wilkins 223 Itoh et al J Thorac Imaging • Volume 19, Number 4, October 2004 FIGURE 7. A, A lateral view of a double-layered alveolar sheet. Note every lateral wall of the alveolus adjoins the apex of the alveolar dome. B, Histology confirms that the doublelayered alveolar sheets hold alveolar domes in common. FIGURE 8. A, Histologic specimen shows a network in the parenchymal space that surrounds the alveolar ductal lumen. Note that every alveolar duct appears isolated. B, Magnified view of the inflated and fixed lung specimen showing frequent branching of the alveolar duct. FIGURE 9. A, Contact radiograph of alveolar ducts with barium sulfate. Note the round radiolucent area corresponding to alveolar ductal lumen surrounded by polygonal alveoli. B, Note the cylindrically-shaped bronchioles and polygonal shape of the alveolar duct. C, On histology, a greater number of alveolar ducts are shown compared with those seen in a bronchiole. 224 © 2004 Lippincott Williams & Wilkins J Thorac Imaging • Volume 19, Number 4, October 2004 Architecture of the Lung FIGURE 10. A, Contact radiograph of respiratory bronchiole with barium sulfate, showing an increase in the number of alveoli as the respiratory bronchiole branches out. B, Note the constant distance from respiratory bronchiole to the nearest septal structures of the secondary lobule. C, Histology of the respiratory bronchiole. D, Magnified view of the respiratory bronchiole demonstrating the double sheet of alveoli abutting the recurrent branch of alveolar duct. Typically, small pulmonary vessels are located in the corner where 4 alveolar ducts gather (Fig. 12C). This corner is called a ridge in solid geometry and is ideal for blood vessel distribution. However, we do not know the specific details of how the arteriole and venule are arranged in lung parenchyma. For this purpose, radiologic analysis combined with 3-dimensional reconstructions may be necessary. The rough arrangement of the arteriole and venule within the secondary lobule is shown in Figure 12D. However, the size of these vessels is still too large to study at an alveolar ductal level. FIGURE 11. A, Micrograph demonstrating a dense network of alveolar capillaries consisting of a number of irregular polygons. B, Magnified view of the lung parenchyma shows a number of alveoli abutting the pulmonary vein (arrow). C, Histologic specimen shows contact between alveoli and pulmonary vein. © 2004 Lippincott Williams & Wilkins 225 Itoh et al FIGURE 12. A, Micrograph shows connection between alveolar capillaries and post- or pre- capillary small vessels. B, Magnified view of the lung shows small pulmonary vessels occupying part of the limited interstitial space between alveolar ducts. C, Histology shows typical location of small pulmonary vessel. D, The contact radiograph shows rough arrangement of arteriole and venule within the secondary lobule. FIGURE 13. A, Macroscopic specimen of the left lower lobe inflated with air. B, 3D CT of the specimen. Note the rich network pattern especially in the lower portion. C, HRCT shows subpleural structure as thin lines along visceral pleura. D, Histology confirms subpleural lymphatics. J Thorac Imaging • Volume 19, Number 4, October 2004 J Thorac Imaging • Volume 19, Number 4, October 2004 BRONCHIAL CIRCULATION There is a rich blood supply from bronchial arteries in the bronchi and hilar lymph nodes as well as communicating vessels between the pulmonary vein and the bronchial venous plexus.5 Bronchial veins are located around a bronchoarterial sheath, which communicates directly with the adjacent pulmonary vein. The pulmonary vein gives off a small branch to the neighboring airways. This special route may be responsible for peribronchial cuffing seen in the abnormal condition where pulmonary venous pressure elevates. PULMONARY LYMPHATICS Subpleural lymphatic structures are sandwiched between air and lung parenchyma. As shown in Figure 13, 3-dimensional CT shows these structures to be a rich network, especially in the lower portion of the specimen. On HRCT, they appear as thin lines along the visceral pleura (Fig. 13C). Finally, these subpleural lymphatics were proved on histology (Fig. 13D). CONCLUSIONS Knowledge of the architecture of lung parenchyma is essential for understanding the morphologic-functional relation- © 2004 Lippincott Williams & Wilkins Architecture of the Lung ship of the lung to elucidate the gas exchange process. The lung parenchyma is mainly comprised of numerous aircontaining passages and intervening fine structures, corresponding to alveolar ductal lumens and alveoli, whose shapes and relative arrangements in 3 dimensions were discussed in detail. ACKNOWLEDGMENT The authors thank Ms. Donna Wolfe, Mr. Michael Larson, and Mr. Ronald J. Kukla for their assistance in manuscript preparation. REFERENCES 1. Itoh H, Nakatsu M, Yoxtheimer LM, et al. 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