Distribution of Bronchial Arteries in the Human Lung K. K. Pump, M.D., F.C.C.P.
Corrosion models of two aged human lungs were prepared by injecting the bronchial arteries, the pulmOl18l'Y artery and vein lIS weD as the tracheobronchial tree with colored latex, using a different color for each system. The bronchial arteries, in particular, were studied by microdissection. Two types of anastomoses which occur between the bronchial and the pulmonary arterial vessels are described. One type, which involves vessels of larger caliber were found primarily on bronchi with diameters ranging from 1.60 mm to 3.5 mm whereas the other variety which consists of precapiUary-sized arterioles was seen within or on the surface of lobules. Branches of the bronchial artery proceeded to the parenchyma where they formed a capillary network which merged with that of the pulmonary artery. The anatomy and physiology of the bronchial arteries has been discussed.
I n surveying the literature dealing with the history
of the bronchial arteries, one is impressed by the length of time and the range of disciplines that have been needed to comprehend an apparently simple system that was merely supposed to nourish the coats of the great airways and their accompanying vessels. Although anastomoses between pulmonary and bronchial arteries were first seen by Ruysch' in 1721, it took another 135 years and the genius of Virchow to show that the bronchial circulation could sustain portions of the lung parenchyma long after the pulmonary arteries had been occluded. 2 Subsequently, early reconstructions of the pulmonary plexus in human embryos by Congdon" seemed to support Virchow's thesis, since from the beginning the pulmonary plexus appeared to be supplied by pulmonary and systemic arteries. This lent support to the extensive system of pulmonary anastomoses described by Weibel" in the adult human lung. Then, in 1970, it was discovered by Boyden" that bronchial arteries, per se, do not appear until the ninth to twelfth week of gestation, ie, long after the pulmonary circulation has been established. Slowly, after sprouting from the aorta and intercostals, these arterials grow down the bronchial tree like parasitic creepers, keeping pace with cartilage formation and establishing capillary connections with the pulmonary circulation. So, as a Reprint requests: Dr. Pump, 5550 Kingston Road, Vancouver 8, BC, Canada
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further complication, it appears that anastomoses, too, have to undergo development. Strangely enough, the pioneer American student of pulmonary structure in man, W. S. Miller," never accepted the existence of arterial anastomoses in the lung. Very recently, Cudkowiez" also has denied their existence, stating that bronchial arterioles which serve as vasa varsorum for pulmonary arteries may under pathologic conditions become the principal pathway for the establishment of bronchopulmonary precapillary anastomoses. However, 18 among others, have described numerous anastomoses between bronchial and pulmonary arteries in the adult lung. These were demonstrated in corrosion models of the human lung in which bronchial and pulmonary arteries had been injected with diHerently colored latex solutions. In such preparations, anastomotic connections ranged in diameter from 0.05 to 0.5 mm and in length from 0.1 to 10 mm. In the present article attention has been focussed on the so-called "bronchopulmonary arteries"-those branches of the bronchial artery that terminate around the alveoli in the capillary plexuses of the parenchyma. This precise localization was made possible by the recently detailed analysis of the surface topography of the pulmonary acini-the clusters of end branches of the bronchial tree." Very recently this study of the exterior has been supplemented by Boyden's'? precise histologic reconstruc-
447
K. K. PUMP
448 tion of the pulmonary acinus as viewed from inside the air ways. So the way is now paved for mapping the distribution of bronchopulmonary arterioles.
Further details of the method are contained in previous publications. 8,9,11
METHOD
The bronchial arteries, which usually arise from the aorta or intercostal arteries 5 •12 ,13 pursued a rather tortuous, serpentine course along the surface of the bronchi. Even peripherally it was common to see two bronchial arteries for each bronchus. At the hilum the bronchial artery had a diameter of approximately 1.5 mm, but was diminished to 0.5 mm to 0.75 mm at point of entry into a segment. Numerous branches were given off at the hilum, some of which proceeded to the pericardium and esophagus, whereas others were destined for the mediastinal pleura. A rich collateral circulation with other systemic arterial vessels was evident in the mediastinal region. A bronchial artery at times deviated from its usual course on the surface of a bronchus, assumed a position on or alongside a pulmonary artery or vein. Thus in one instance a bronchial artery pursued a winding course around a pulmonary vein for a distance of 35 mm. The bronchial arteries supplied nutrient
For this study the left lungs of two elderly men (ages 78 and 80), who had not had any respiratory complaints, were used. Both lungs, on the basis of histologic and corrosion model examination, were classified as aged lungs. The findings in this report were deducted from microdissection of corrosion models prepared of both lungs. The models were prepared by using Vultex moulage," a latex, as the injection medium. The first concern was to find the bronchial arteries. To anticipate anomalous origins, the first five intercostal arteries were dissected free, tied off and severed 5 cm from their aortic origin. Then the left lung, intercostal arteries and aorta were carefully removed from the thorax, care being taken not to tear the bronchial arteries. As soon as one was found-in both left lungs they arose from the aorta-it was dissected free for a distance of a few centimeters. After cannulating the bronchial artery with a 20-gauge needle, it was injected with bright green latex. A syringe was used for the injection. The pulmonary artery was then injected with blue and the pulmonary vein with brown Vultex moulage. The tracheobronchial tree was injected last with white Vultex moulage. ·Obtained from General Latex and Chemicals (Canada) Ltd., Brampton, Ontario.
Pulmonary vein--- - --, Vasa vasorum to pulm. vein
OBSERVA nONS
--~--
BR O N C H I A l
ARTERIES
/ Pulmonary artery / / Broncho- pulm. art. anast. /vasa vasorum to pulm. art. Broncho- pu Imonary art. Pulmo-bronchial art.
*Precapillary anastomosis FIGURE 1. Composite drawing of dissected specimens demonstrating the relationship of the bronchial artery and its branches to the bronchus and its subdivisions, the pulmonary parenchyma, the pulmonary artery and vein. The inset illustrates the fusion of the bronchial and pulmonary artery capillary networks, both in tum terminating in the venous system. The asterisk draws attention to the existence of anastomoses between the bronchial and pulmonary precapillaries (T.B.-tenninal bronchiole).
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DISTRIBUTION OF BRONCHIAL ARTERIES IN THE HUMAN LUNG branches to the bronchi, vasa vasorum to the pulmonary arteries as well as to the veins and numerous bronchopulmonary branches to the parenchyma of the lung. An assembly drawing illustrating relationships at the periphery of the lung is shown in Figure 1. Measurements of the diameters of the bronchial arteries and their respective bronchi were made to determine whether a relationship existed between the dimensions of their lumina. Since a bronchus may have more than one bronchial artery this estimation was difficult to establish. In 18 such measurements, including bronchi with diameters ranging from 0.8 mm to 5 mm the ratios of the bronchial diameter to that of the bronchial artery varied from 3: 1 to 18:1. Sixty percent had a ratio between 3:1 to 8:1. Many segmental bronchial arteries were dissected to determine their mode of termination. In most instances the bronchial artery terminated by dividing into bronchopulmonary branches at a point several divisions proximal to the terminal bronchiole. In two instances, however, the bronchial artery proceeded up to the preterminal bronchiole where it divided into bronchopulmonary branches. The latter merged into nearby alveolar clusters to form a capillary network (Fig 4). In no instance did we see the bronchial artery contlhue into an acinus along the route of the acinar arteriole, ie alongside the terminal and the subsequent respiratory bronchioles. Bronchopulmonary branches were given off throughout the course of the bronchial artery. Such branches as a rule, proceeded to a lobule in its immediate vicinity where they continued to divide to form a capillary network (Fig 1 and 2). The method of formation of the capillary network, contrary to that of the pulmonary arteriole" had no recognizable pattern. Once reaching the lobule the bronchopulmonary branch either dipped into its substance and there broke up into capillaries or it branched repeatedly on the surface of the lobule until the capillary network was established. Dissections did show that this capillary network merged or anastomosed with the capillary network of the pulmonary artery (Fig 1). The appearance in the pulmonary vein of the green latex used for the injection of the bronchial artery also testified to the correctness of this finding. The capillaries arising from the bronchopulmonary branches had the same diameter, namely 4.3 /I- to 8.6/1- as the capillaries from the pulmonary artery.'! Toward the periphery of the lung the bronchopulmonary branches became more numerous and their diameter diminished in size. The length of
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FIGURE 2. Photograph demonstrating a branch of the bronchial artery (green) giving off a bronchopulmonary branch to the pulmonary parenchyma (white) as the artery proceeds across a pulmonary vein (brown). Note the vasa vasorum from the bronchial artery to the pulmonary vein. Magnification 10 X.
these branches varied from 1.75 mm to 22.5 mm, whereas the diameter ranged from 72/1- to 125/1-. To establish the frequency of bronchopulmonary branchings four segmental bronchi with their bronchial arteries were dissected in detail. In the 78-year-old lung the average distance between bronchopulmonary branches was 5 mm, but this decreased to 2.5 mm in the peripheral portion of the lung. In the 80-year-old lung these branches appeared to be even more numerous, with an average distance of 2 mm between branches. These distances were only average as in many instances the branches arose in groups of three and four. A greater preponderance of the bronchopulmonary branches reduced their diameter correspondingly. In the dissection of these lungs two types of bronchopulmonary arterial anastomoses were encountered (Fig 1 ). The first type involved branches of the pulmonary and bronchial arteries 19cated on bronchi with diameters ranging from 1.60 mm to 3.50 mm. The diameter of the bronchial arteries in this type of anastomosis measured from 72/1- to 325/1-. The anastomoses were end to end or end to
FIGURE 3. Photograph illustrating precapillary anastomosis between the bronchopulmonary (green) and pulmonary arteries (blue). Diameter of vessels approximately 25 microns. Alveoli in background.
K. K. PUMP
450 side. This type of bronchopulmonary arterial anastomosis, referred to by von Hayek's as "Sperrarterien," have been described in greater detail in a previous publication." The second type of anastomosis, which could also be end to end or end to side, occurred between precapillary sized bronchopulmonary and pulmonary arterial vessels with diameters ranging from 24ft to 48ft (Fig 3). They were usually found on the surface or within pulmonary lobules. This type of anastomosis according to Robertson" is not of the "Sperrarterien" type. On occasions bronchopulmonary arterial anastomoses of quite small diameter were also found on the surface of bronchioles. The parent branch of the pulmonary arterial vessel in such instances was a pulmobronchial artery, so called because after supplying several branches to a bronchiole it proceeds to the alveolar parenchyma 16 ( Fig 1 ). Similar anastomoses were also encountered where the small twigs of the two types of arteries were lying on a pulmonary vein. In addition to supplying small branches for anastomoses the bronchial artery while on the vein, also gave off vasa vasorum to the pulmonary vein wall (Fig 2). Von Hayek'! also claims that there are anastomoses between precapillary-sized bronchial artery and pulmonary vein vessels, occurring primarily in
Broncho- pulmonary arteries
1.0 ,mm
Bronchia I arter)
FIGURE 4. Drawing of a dissected specimen illustrating the tennination of a branch of the bronchial artery by breaking up into bronchopulmonary branches before reaching the terminal bronchioles (T.B.-tenninal bronchiole).
the pleura and within the bronchial walls. Corrosion models are inadequate for the demonstration of such anastomoses. DISCUSSION
The function of the bronchial arteries is obviously not limited to providing nutrition for the walls of the bronchi, pulmonary arteries and veins, the mediastinal lymph nodes and septal tissues. The presence of anastomoses with the pulmonary arteries and the response in the form of hypertrophy to certain pathologic conditions and congenital cardiac abnormalities indicates that the bronchial arteries perform a vital, adaptable funotion.Fr'" By selective opening of the arterial bronchopulmonary anastomoses the oxygenated blood of the bronchial arteries can be directed to specific areas of ischemic lung tissue. Lapp'" also suggested that these anastomoses have, in all probability, an important physiologic function in regulating blood How in the lesser circulation. During inspiration, he suggested, blood flows from the bronchial into the pulmonary arterial system since the blood pressure drops in the pulmonary artery during inspiration. Furthermore, more blood is directed through the anastomoses toward the pulmonary artery to poorly ventilated or atelectatic areas in order to feed the parenchyma where its own capillaries would not carry oxygenated blood. The blood How through the anastomosis, in his opinion, is therefore not only dependent on differences in pressure in the two systems but also dependent on the need for oxygen. It is probable, therefore, that a physiologic need governs the How through the anastomoses. If the physiologic need surpasses the capacity of the "normal" bronchial arteries, as in cases of pulmonary stenosis, the bronchial arteries may be reinforced by collateral vessels.F The function of the bronchopulmonary branches, their precapillary anastomoses and capillary networks is difficult to define. The suggestion by Lapp'" that this blood is to nourish the alveolar septal membranes designates to them a rather limited function, since all blood at the alveolar level is capable of supplying the necessary oxygen. It may well be that the bronchopulmonary branches represent a system of vessels particularly adaptable for supplying oxygenated blood to areas which are afBicted with infections or other abnormal conditions. Infections of the pulmonary parenchyma, especially pneumonias, produce an avascularity of the pulmonary arterial territory in the lung segments or lobes affected. This state, according to Wagner," is not restored to normal for several
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DISTRIBUTION OF BRONCHIAL ARTERIES IN THE HUMAN LUNG
weeks or months after apparent clinical cure. Mathes" as well as Karsner maintain that such areas are perfused by bronchial arterial blood derived from considerably dilated bronchial arteries leading to the areas of consolidation. The bronchopulmonary branches and their numerous precapillary-sized anastomoses with pulmonary arterial vessels would under such circumstances playa vital role. Tyler and assoeiates'" advances the hypothesis that the alveolar bronchial artery supply through the bronchopulmonary branches serves the nutritive requirements of an increased amount of supportive tissue in the region of the alveolus. Since this tissue is not primarily diffusing in nature it has to obtain its nutrition by other means. They further postulate that if this hypothesis is true, the possibility exists that an occlusive lesion of the bronchial arteries might cause widespread degeneration of supportive tissue similar to that seen in generalized emphysema. Although the two lungs studied were aged lungs, which implies that they had a mild nonobstructive emphysema, the bronchial arteries did not appear abnormal. The same conclusion was reached by Miyazawa and co-workers," who studied bronchial Bow in emphysema by means of bronchial catheterization. Boyden" in his study of the embryology of the bronchial arteries has evidence which suggests that the development of the bronchial arterial system is not completed much before the time when the fetus becomes viable. This would imply that at least early in life the viability of the pulmonary parenchyma is not dependent on the bronchial arteries. If the pressure in the capillaries arising from the bronchopulmonary arteries is higher than in those originating from the pulmonary arteries then the bronchial arterial blood would be better suited to perfuse the abnormal tissues as seen in the various pulmonary fibroses, in Hamman-Rich syndrome and in various tumors or granulomas. Several authors l 9 •21 claim that the bronchial arteries continue peripherally as far as the respiratory bronchioles. Our dissections have not confirmed this, for we found the bronchial artery to terminate at least one to several divisions proximal to the terminal bronchiole by dividing into bronchopulmonary branches which proceeded to nearby clusters of alveoli to form a capillary network (Fig 4). ACKNOWLEDGMENT: For the expert and skillful drawings rendered by Miss Marguerite Drummond, Medical Artist of the University of British Columbia, I am most grateful. The Autopsy Service of the Shaughnessy Veterans Hospital, Vancouver, BC has been very helpful in supplying us with
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necropsy material. Materials and equipment were supplied through the Medical Research Council of Canada, Grant-inAid M.A. 1323. REFERENCES
1 Ruysch F: Opera omnia. Amstelod: Tom 1, Epist Anat Sexta, 1721 2 Virchow R: Weitere Untersuchungen tiber die Verstopfung der Lungenarterie und ihre Folgen, Gesammelte Abhandlungen zur Wissenschaftlichen Medizin. Frankfurt AM, 1856 3 Congdon ED: Transformation of the aortic-arch system during the development of the human embryo, Contrib Embryol (No. 68) Carnegie Inst 14:47,1922 4 Weibel E: Die Blutgefassanastomosen in der menschlichen lunge. Z Zellforsch 50:163,1959 5 Boyden EA: The Developing Bronchial Arteries in a Fetus of the Twelfth Week. Amer J Anat 129:357, 1970 6 Miller WS: The Lung ed 2. Springfield, Illinois, Thomas, 1947 7a Cudkowicz L: The Human Bronchial Circulation in Health and Disease. Baltimore, Williams & Wilkins Co., 1968 7b Cited by Cudkowicz, L 8 Pump KK: The bronchial arteries and their anastomoses in the human lung. Dis Chest 43:245,1963 9 Pump KK: Morphology of the acinus of the human lung. Dis Chest 56:126,1969 10 Boyden EA: The structure of the pulmonary acinus in a child of six years and eight months. Am J Anat 132:275, 1971 11 Pump KK: The circulation in the peripheral parts of the human lung. Dis Chest 49: 119, 1966 12 Liebow AA: Patterns of origin and distribution of the major bronchial arteries in man. Am J Anat 117:19,
1965
13 Cauldwell EW, Siekert RG, Liniger RE, et al: The bronchial arteries. An anatomic study of 150 human cadavers. Surg Gynec Obstet 86:395, 1948 14 Hayek Hv: Die MenschIiche Lunge. Berlin, SpringerVerlag. English Translation: Krahl VE The Human Lung. New York, Hafner Publishing Co, Inc, 1960 15 Robertson C: The intrapulmonary arterial pattern in infants with transposition of the great arteries associated with interventricular system defect. Virchows Arch Path Anat P 344:230, 1968 16 Wagenvoort CA, Wagenvoort N: Arterial anastomoses, bronchopulmonary arteries and pulmobronchial arteries in perinatal lungs. Lab Invest 16: 13, 1967 17 Liebow AA, Hales MR, Lindskag GE: Englargernent of the bronchial arteries and their anastomoses with the pulmonary arteries in bronchiectasis. Am J Clin Path 25:211, 1949 18 Miyazawa K, Katori R, et al: Selective bronchial arteriography and bronchial blood flow: Correlative study. Chest 57 :416, 1970 19 Lapp H: Uber die sperrarterien der Lunge und die Anastomosen zwischen A. Bronchialis und A. Pulmonalis, uber ihre Bedeutung, insbesondere fur die Entstehung des Haemorrhagischen Infarktes. Frankfurt Z Path 62: 537, 1951 20 Tyler WS, McLaughlin RF, Canada RO: Structural analogues of the respiratory system. Arch Envir Hlth 14:62, 1967 21 Tobin CE: The bronchial arteries and their connections with other vessels in the human lung. Surg Gynec Obstet 95:741, 1952