On the purported discovery of the bronchial circulation by Leonardo da Vinci.

On the purported

discovery of the bronchial by Leonardo da Vinci WAYNE MITZNER AND The Johns Hopkins Medical

ELIZABETH Institutions,

WAGNER Baltimore, Maryland

MITZNER, WAYNE, AND ELIZABETH WAGNER. On thepurported discovery of the bronchial circulation by Leonardo da Vinci. J. Appl. Physiol. 73(3): 1196-1201, 1992.-Among modern physiologists and anatomists, there has been a nearly universal acceptance that Leonardo da Vinci was the first to identify the anatomy of the bronchial circulation. However, because of certain ambiguities in both his anatomic drawing that was supposed to have shown this circulation and the accompanying descriptive text, we questioned whether he really could have been the first to discover this small but important vasculature. To address this question, we set out to repeat Leonardo’s dissections in the ox. We reasoned that perhaps the normally tiny bronchial vessels would be considerably more noticeable in this very large species. Our dissections, however, failed to provide any evidence that Leonardo’s drawing was that of the bronchial circulation. Furthermore we observed a set of distinct small pulmonary veins to the left upper and right middle lobes that Leonardo, given his lack of understanding of the function of the lung and its circulation, could have easily mistaken for a separate circulation. We thus conclude that Leonardo da Vinci did not describe the anatomy of the bronchial circulation. We believe that the first person to clearly and unequivocally describe the anatomy of this circulation was the Dutch Professor of Anatomy and Botany, Frederich Ruysch. pulmonary veins; bronchial ich Ruysch

artery;

airway

circulation;

Freder-

that LeonardodaVinciwas the first to discover the existence of the bronchial circulation. The first modern reference to this discovery is in McMurrich’s book on Leonardo’s anatomic drawings (8). In discussing the figure shown in Fig. 1, McMurrich states that “Leonardo probably discovered the bronchial circulation” (emphasis added). The fact that the word probably was included in this statement indicated that the author had some doubt about this conjecture. However, for reasons that are not entirely clear, all later historical authors (2, 3, 6, 7, 9) seemed to have lost this doubt. Indeed, Keele (6) indicated that this might have been one of Leonardo’s most important discoveries. We hope to show that the caution that McMurrich expressed was well justified and that it is very unlikely that Leonardo discovered or described the anatomy of the bronchial circulation. First, we will present what Leonardo knew about the circulation of blood and, second, we will repeat his experimental work and describe what he likely saw with his experimental dissections. Figure 1 shows the famous picture (Q II, 1R) in the Quaderni d’anatomia (11) that has given rise to the misITISGENERALLYACCEPTED

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understanding. When the picture is viewed by itself, without text, it seems unlikely that anyone would have taken this circulation to be the bronchial. First, the bronchial arteries do not consistently run along the dorsal side of the tree. The arteries run laterally, more or less between the bronchus and the pulmonary artery. Second, the bronchial arteries arise from the descending aorta, not from the structure shown in the figure, which later will be demonstrated to be the left atrium. Third, and perhaps most importantly, Fig. 2 reproduces another drawing by Leonardo (Q II, 2v) showing the pulmonary venous tree, viewed from the same dorsal perspective, and arising from the same part of the heart as the presumed bronchial circulation. Thus, the vasculature in Fig. 1 could well be a part of the pulmonary venous circulation. Thus, by itself without text, the circulation drawn in Fig. 1 would never have been interpreted to be bronchial circulation. The confusion that has arisen derives from the text that is associated with the figure. Although much of the text on this page does not relate directly to the drawing, two important sections are relevant to the present discussion. The first is a somewhat ironic cautionary warning about taking what he writes too seriously. It starts at the lower right of the heart and continues directly below the heart. The following is the English translation from Ref. 10 Oh Writer, with what words will you describe with like perfection the entire configuration as the design here makes? This you describe confusedly, having no knowledge, and you leave little knowledge of the true forms of the things, which you, auditor, having to speak of the configuration of any corporeal thing surrounded by superficies. But I remind you not to involve yourself in words, if you do not speak to the blind; or if nevertheless you will demonstrate with words to the ears and not to the eyes of men, speak of substantial or natural things and do not meddle with things appertaining to the eyes, making them enter by the ears, as you will be by far surpassed by the work of the painter . . . the longer you write, minutely, the more you will confuse the mind of the auditor.

Thus, Leonardo himself is telling us not to take what he writes too seriously. In this context, it should be noted that Leonardo himself contributed to the difficulties associated with interpreting the written word by being an erratic phonetic speller and by omitting punctuation from his writings (7). The second relevant and oftenquoted passage appears on the lower right below the drawings of the trachea and main stem bronchi. In Leon-

0 1992 the American

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LEONARDO

FIG.

1. Leonardo’s drawing of purported

DA

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bronchial circulation.

ardo’s time the term “trachea” was used to refer to the entire airway tree and “venarteria” was the term for pulmonary vein. A translation of this passage follows The artery lies below the vein; it is true that some of its branches sometimeslie above the vein. Reminder You have to consider

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ies and veins. However, as will be argued later, these could just as well be a smaller set of pulmonary venous branches. In addition, it must be emphasized that, unlike the vascular supply to most organs (including the pulmonary circulation in species that Leonardo dissected), there are no bronchial veins accompanying bronchial arteries. Thus, if Leonardo’s picture and text do in fact refer to such bronchial veins, it is clear that they could have only been drawn from his imagination. What Leonardo means when he speaks of vessels, “one above the other,” is also unclear. It has been interpreted as referring to the pulmonary and bronchial circulations, but it could also be a reference to the fact that, in the animal species Leonardo dissected, the bronchus has a pulmonary artery on one side and a pulmonary vein on the other or, in other words, one above the other. This interpretation is supported by the statement that immediately precedes the Reminder, indicating no small degree of uncertainty on Leonardo’s part. Leonardo also speaks of larger and smaller vessels, and this may in fact again be a reference to different-sized pulmonary veins. Nevertheless, despite these ambiguities with the text describing the anatomy, the passage does seem to convey the general function of what we know as the bronchial circulation. Another section of the drawing in Fig. 1 has been used by some authors to support evidence of Leonardo’s discovery of the bronchial circulation. This argument is related to the depiction of an abscess at the bottom of the lung in Fig. 1 (1, 2). There is also a line connected to a small section of text that briefly describes this abscessas a hard callus filled with dust and fluid and formed in small airway branches. However, nothing is said about the circulation to this abscess,nor is there any indication that the circulation shown in the drawing connects to it. The tubular connection to the abscessshown is in fact a cartilaginous airway. The fact that we now know that such abscessesoften are perfused from the systemic circulation (1) is not relevant. We can give Leonardo credit for describing and depicting a pulmonary abscess, but

the second degree of the veins

and arteries which coat the first minute veins and arteries that nourish and vivify the trachea, which substance that is which interposesitself between the first and the 2nd veins and arteries, and why Nature duplicated artery and vein in such instrument, one above the other, finding themselves for the nourishment of one and the same member-you may say that the trachea and the lung had

to be nourished; and if you had to do with a single large venarteria, this could not bejoined to the trachea without great impediment of the movement which the trachea has in its increasing and diminishing, as well lengthwise as crosswise, wherefore for this Nature gave the trachea such veins and artery that were sufficient for its life and nourishment, and somewhat removed the other large

branchesfrom such trachea, to nourish the substanceof the lung with greater convenience. There are several ambiguities with this text, and various authors have applied their own interpretations. Both O’Malley and Saunders (9) and Keele (6) considered vessels of the first order to mean the bronchial arter-

FIG.

2. Leonardo’s drawing of pulmonary venous tree.


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there is no reason to believe that he knew anything about its vascular anatomy. To begin to analyze the meaning of the Reminder describing the circulation in Fig. 1, let us first consider what Leonardo knew and understood about the circulation. The fact that is generally accepted among Leonardo scholars is that he knew nothing about the circulation of blood (6, 8). It may seem surprising that such a superb engineer, who drew accurate pictures of the valves in the heart, could not figure out which way blood flowed. However, Leonardo was never able to free himself from Galens concept of the ebb-and-flow model of the circulation. Indeed, Galen’s concept led Leonardo to depict structures artistically that were not there. Thus, Leonardo knew that the ventricular septum had many holes in it and functioned as a sieve, shunting blood back and forth between the ventricles. He knew this not because he saw the septal holes, but because this is what Galen had taught (8). Leonardo drew several pictures of the septum that included these essential holes. Thus, at least in this instance, Leonardo’s scientific judgment was clouded by this well-entrenched model. As another example, Leonardo believed that, as a general principle, arteries and veins and nerves always travel together. Thus, in another figure (Q II, 2R), he drew a picture of the trachea with a branching nerve supply. Although nerves certainly do follow the airway tree, they are even less visible to the naked eye than the bronchial arteries. He apparently saw the vagus nerve running along the dorsal side of the lower trachea, with branches coursing around the carina in their passage to the heart, and transcribed this to be consistent with his model. Thus, despite his considerable genius, Leonardo was still limited by the existing intellectual environment. George Sarton (S), perhaps the leading scientific historian of his day, stated it very nicely in his introduction to McMurrich’s book on Leonardo’s anatomic studies Galen’s triumphant dogmatism made even a Leonardo see the inexistent. But for this illusion which sidetracked him hopelessly, Leonardo might conceivably have discovered the circulation of the blood before Harvey, for he had as much anatomical and mechanical knowledge as was needed. He had all that was necessary to see the truth, except that in this particular case he was blinded by an overpowering prejudice. One could not illustrate better the limitations of genius. A man of genius sees further than his fellowmen, further and more clearly, but for all that his range of vision is limited. Leonardo was an extraordinary man, yet he belonged to his environment-fifteenth century Italy-almost as completely as his humbler contemporaries. What else could we expect? This father of modern science was still in many respects a child of the Middle Ages.

The question remains as to how Leonardo could have discovered such tiny bronchial arteries, which are often difficult to find today under the best of conditions, even with the knowledge that they do exist. Indeed, we know that the conditions under which he worked were far from ideal. His dissections were done on decaying organs in the evening under candlelight. He himself makes a note of some of the problems (6, p. 197)

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And though you have love for such things you will perhaps be hindered by your stomach; and if that does not impede you, you will perhaps be impeded by the fear of living through the night hours in the company of quartered and flayed corpses fearful to behold.

From further reading of his works, it occurred to us that perhaps it was simply a question of size. Much current work is done in 20- to 30-kg dogs and 30- to 60-kg sheep. The dissections on which Leonardo based his drawings are reported1 to have been carried out during his later years in Rome, on the heart and lungs of oxen obtained from the local abattoir (6). We questioned whether the bronchial vessels in a 600-kg ox might be an order of magnitude greater than that normally seen in a 30-kg sheep. To repeat his experiment, we obtained hearts and lungs of three separate oxen from the local Baltimore abattoir. On three occasions, we received the heart and lungs after a skilled butcher killed the ox by rapid exsanguination through severed carotid arteries. The removal of the heart and lungs was also done by the butcher, because regulations prevented us from doing the surgery ourselves. The three specimens showed similar anatomy, at least to the extent that we dissected them. The origin of the bronchial artery from the bronchoesophageal artery was very similar to that described in the-sheep. In addition to the bronchial artery, the bronchoesophageal artery gave rise to an esophageal branch and one or two smaller branches directed cephalad. With knowledge of the sheep anatomy and further dissection, we identified the bronchial artery as it approached the main stem bronchi from the aorta. However, to our disappointment, the artery was only about twice as large as that in the much smaller sheep. Apparently, much of the increased weight of the ox is not reflected in the size of the lung and its vasculature. ’ This raises another issue that will be only mentioned briefly here. Nearly all scholars who have written on Leonardo’s anatomic drawings assume that his later thoracic drawings arise from dissections in the ox. Furthermore, his earlier drawings showing the heart and lungs are reported in his notes to be based on dissections in the pig (6, 9). Of particular interest is his drawing of the bronchial tree as a very symmetrical dichotomous branched structure in a three-dimensional perspective (K/P 53 v). What is puzzling with regard to these drawings of the lungs based on both the ox and pig is the complete absence of any representation of the bronchus to the right upper lobe. In both species this unique bronchus arises from the trachea above the carina. There are several possible explanations for his failure to have drawn this bronchus. Perhaps he deliberately omitted it, as Keele and Pedretti (7) suggest, because it upset his strong sense of symmetry or because he attempted to adapt his animal studies to human anatomy. It is also conceivable that he never noticed this branch. The right upper lobe is generally tightly apposed to the trachea, and unless an effort was made to dissect it away, the bronchus could have been overlooked. Finally, one must consider that his dissections of the lung airway tree were not based on the above two species. Perhaps he dissected rat lungs and then applied his anatomic insights to his drawings of other species. This may be reasonable, because it is believed that most of his anatomic drawings were done from memory after the dissection was completed. In this regard, Keele’s comment regarding some of Leonardo’s errors in his drawings of the skeletal system seems quite relevant (Ref. 6, p. 24): “This and other similar examples once again emphasize the danger of allowing the excellence of the draughtsman to hide the deficiencies of the anatomist.” Nevertheless in our present work we have assumed that he did indeed do his dissections in the ox, because, if he worked in any smaller species, it would be even less likely that he could have seen the bronchial vasculature.


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FIG. 3. Left: photograph showing right pulmonary vein (indicated by hemostat) going to right middle lobe. Right lung is pulled slightly downward. Right: artistic rendering of photograph at left. Pulmonary vein to right middle lobe and pulmonary vein to left upper lobe were identified with further dissection. Note fat pad overlying left atrium in photograph and its clear demarcation, giving it superficial appearance of a large vessel into which above small pulmonary veins enter.

We next located and cannulated the origin of the bronchoesophageal artery in the descending aorta and injected a contrast medium to enable more careful dissection. In this regard, there is no evidence that Leonardo ever injected such a contrast material to trace any of the vascular trees he drew, nor does there exist any drawing of his of the cardiopulmonary vasculature that also includes the relevant part of the descending aorta. With injection of contrast material, however, we could clearly observe the entire anatomy of the bronchial vasculature as it approaches the main stem bronchi from the descending aorta and along the airway tree. Seeing the small size of these vessels and their anatomic location along the medial surface of the airways enhanced our skepticism that Leonardo could have seen these vessels at the carina and then followed them down the airways, as his picture shows. However, in our dissection of these bronchial arteries, we noticed a somewhat unique anatomy that might explain what Leonardo saw. In the ox, there are distinct small pulmonary veins that arise from the dorsal side of the left atrium and then travel obliquely along the main stem bronchi. One such vessel going to the right middle lobe is shown in Fig. 3. The main pulmonary venous branches in most species normally enter the atrium more on the ventromedial side of the trachea and main stem bronchi. However, the pulmonary veins of the ox are somewhat unique in this pulmonary venous anatomy, perhaps because of the branching pattern of the bronchial tree structure. The ox lung has two bronchi coming off the distal end of the trachea, almost immediately at the carina (5). These branches go to the right middle lobe and the left upper lobe. The pulmonary veins that drain these lobes arise from the dorsal side of the main stem bronchi, cross them at an oblique angle, and continue along the smaller airways. They are quite distinct from the much larger main pulmonary veins that enter at the

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hilum on the medial and ventral side. Figure 3 also shows that these pulmonary veins arise from a region of the heart that looks very much like the same structure from which the supposed bronchial arteries arise (see Fig. 1). The fat pad that overlies the dorsal side of the left atrium gives it an appearance much like an ascending vessel. Figure 4 shows an anatomic drawing based on sequential photographs of the actual dissection. In viewing both the bronchial vasculature and pulmonary veins shown in Fig. 4, the bronchial artery can be seen clearly arising from the descending aorta. It does not arise directly from the heart, and it does not appear to be as Leonardo has drawn. With regard to the interpretation of Leonardo’s drawing, it is important to note that few authors have recognized that the structure on the left side, from which the supposed bronchial artery arises, is in fact the left atrium. McMurrich (8) writes that “His figure shows two bronchial arteries arising apparently from the aortic arch.” Confounding the situation is the statement by Cudkowicz (2) that the picture shows the aortic origin of the left bronchial arteries, noting that the picture is a mirror image drawing. Apparently, he thought the picture represented a ventral view, whereas in fact it is a dorsal view, with left and right sides clearly labeled by Leonardo. Adding to this confusion is the fact that O’Malley and Saunders (9) identified this structure as the pulmonary artery, stating that “Bronchial arteries n m, spring from the pulmonary to pass to the bifurcation of the trachea.” It must again be emphasized that from the dorsal perspective that Leonardo and we have shown,

FIG. 4. Anatomic drawing based on dissection photographs of bronchial artery and pulmonary veins visible from a dorsal perspective. Bronchial artery was cannulated through descending aorta. Pulmonary veins to right middle and left upper lobes are shown, along with main pulmonary veins that travel down along medial side of main bronchi. Main pulmonary venous trunks are larger than they appear from this drawing, because they extend along medial airway surface around to ventral side.


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it is not possible to see the ascending aorta. Thus, there seems little doubt that the structure from which the supposed bronchial arteries arise in Leonardo’s drawing is the left atrium. To summarize, because these small distinct pulmonary veins to the right middle and left upper lobes start out at least five times the size of the bronchial arteries, they are large enough that Leonardo could have seen them. Because they enter the left atrium separately from the much larger main pulmonary veins that run from the left atrium to the medial and ventral sides of the airways, he might naturally wonder what their purpose was. Without understanding that it might be normal for multiple pulmonary veins to enter the left atrium, he would naturally interpret them to be another set of vessels-they come directly out of the heart, and they are much smaller than either the main pulmonary arteries or veins. They also look more like what Leonardo has drawn in his figure that has been interpreted to be the bronchial arteries, and they are of the proper size. To us it seems inescapable that it is these smaller independent pulmonary veins to the right middle and left upper lobes to which Leonardo refers as the vessels of the first order in his writing. With this new knowledge, we can add the following interpretative annotation to the previous translation regarding Fig. 1

The artery lies below the vein; it is true that some of its branches sometimes lie above the vein. Reminder You have to consider the second degree of the [pulmonary] veins and arteries which coat the first minute [pulmonary] veins and arteries, [all vessels] that nourish and vivify the trachea, which substance that is which interposes itself between the first and the 2nd veins and arteries, and why Nature duplicated [an] artery and [a] vein in such instrument, one above the other, finding themselves for the nourishment of one and the same member-you may say that the trachea and the lung had to be nourished; and if you had to do with a single large pulmonary vein, this could not be joined to the trachea without great impediment of the movement which the trachea has in its increasing and diminishing, as well lengthwise as crosswise, wherefore for this Nature gave the trachea such pulmonary veins and artery that were sufficient for its life and nourishment, and somewhat removed the other large [pulmonary venous] branches from such trachea, to nourish the substance of the lung with greater convenience. In the above context, it thus seems that Leonardo was contemplating how difficult things would be if there were only one single pulmonary vein. Therefore, having seen the unique pulmonary veins of the first order in the ox, Leonardo mistook these for another new type of vessels. Being the great biomedical engineer and modeler that he was, he sought an explanation for the existence of these vessels. Quite strikingly, his model was correct in diagnosing the need for a separate airway circulation, and as already indicated, he even postulated its role. In this context, he therefore excelled as a physiologist but failed as an anatomist. He formulated a function, based on the wrong rationale and structure. He got it right for the wrong reasons. But is it proper then to continue to give him credit for discovering the bronchial circulation? We

,

FIG. 5. Portrait

II

of Frederich

Ruysch.

do not think so. Despite his model describing bronchial circulatory function, he clearly did not discover the bronchial circulation. If not Leonardo, then who was responsible for bringing the existence of the bronchial circulation into the anatomic literature? De Burgh Daly and Hebb (3) cite a passage from Galen, as well as a comment of Galen referring to a comment by Erisastratus (257 B.C.). However, neither of these ancient scholars provided sufficient anatomic description or detail to make one confident that such a relatively hidden circulation was known to them. In 1652, Domenici de Marchettis (1626-1688) published his Armtomia (4); he is considered to be one of the first anatomists to inject a contrast material to show that the smallest arteries and veins were connected. In chapter X, dealing with the heart and lungs, he states The lungs possess arteries and veins, both from the pulmonary artery and to the pulmonary vein, which as we have said permeate the lung. But one can observe two or three arteries which originate in the aorta and propagate through the substance of the lung. . . The sentence continues with details of the nervous innervation and no further mention of the vasculature. However, from this statement, it seems clear that de Marchettis observed some systemic component of the blood flow to the lungs. Unfortunately, there are no drawings or additional discussion that would enable us to


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was also the first to use the designation “bronchial artery.” In his discussion, Ruysch draws a interesting physiological comparison between the lungs and the liver, where there is a portal circulation containing contaminated blood and a much smaller hepatic artery. He then attempts to determine a function of this circulation. Unlike Leonardo, who suggested that a separate vasculature was needed because of mechanical reasons, Ruysch proposed that it was needed to provide a higher quality of blood. He states . . . it is not the quantity but rather the quality of blood that is maximized in the bronchial artery. Who will deny that the blood which flows through the ventricle of the left heart is more distinguished than the blood from the right ventricle. For this reason I believe that, in order to impose a purpose, this artery is created to supply the lungs with more distinguished, more perfect blood, indeed with blood of higher rank. Certainly, for those contemporary scientists investigating the bronchial circulation, this is nothing new. The bronchial circulation has always had such an exalted and primary status.

FIG. 6. Drawing in the article by Ruysch describing bronchial circulation. The following is a translation of legend that accompanies the figure.

Figure IX. Explanation. Illustration of the bronchial tree of a calf from the posterior aspect, denuded of parenchyma, pulmonary veins, and pulmonary arteries, along with the descending aorta cut away from the heart and the bronchial artery. A. Posterior view of the bronchial tree of the calf, cut off from the larynx. B. The right branch. C. The left branch. [Note B and C are mislabeled by Ruysch-they are, in fact, left and right branches, respectively.] D. The bronchial artery, whose branches accompany the bronchi without interruption to their end. E. Posterior part of the descending aorta cut off from the heart, from which the intercostal arteries originate. . intercostal arteries cut off short. F. The upper branch, that I have not found in animals, other than cows and calves.

know just how much beyond this very brief comment he really understood about the bronchial circulatory anatomy and physiology. The Dutch Professor of Anatomy and Botany Frederich Ruysch (1638-1731) (Fig. 5) provided clear and unambiguous evidence regarding the existence of the bronchial circulation in a paper much in the modern format (lo), with a brief literature review, methods, anatomic description, and discussion. He unambiguously described the aortic origins of the bronchial arterial tree and firmly established that this vasculature travels along the bronchi down to the smallest branches. This was illustrated in a detailed drawing reproduced in Fig. 6. His results became widely known and influenced the thinking of subsequent generations of anatomists and physicians. He

We thank Dr. Walter Ehrlich for translating the anatomic works of Ruysch and de Marchettis. We acknowledge the intellectual and spiritual contributions of Dr. John Butler in the writing and critical review of the manuscript. We dedicate this work to his memory. Address for reprint requests: W. Mitzner, Dept. of Environmental Health Sciences, School of Hygiene and Public Health, The Johns Hopkins University, 615 N. Wolfe St., Baltimore, MD 21205. Received 10 February 1992; accepted in final form 13 May 1992. REFERENCES 1. CHARAN,

AND R. DHAND. The role of bronchial in lung abscess. Am. Reu. Respir. Dis. 131: 121-124,

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circulation 1985. 2. CUDKOWICZ,

L. A historical review of the bronchial circulation. In: Bronchial Circulation in Health and Disease. Baltimore, MD: Williams & Wilkins, 1968, chapt. 1, p. l-27. 3. DE BURGH, DALY, I., AND C. HEBB. Pulmonary and Bronchial Vascular Systems. Baltimore, MD: Williams & Wilkins, 1966, chapt. II, p. 42-99. DE MARCHETTIS, D. Anatomia. Patavii: Matthaeum Boltzettam, 1652. The

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KEELE, K. D., AND C. PEDRETTI. Leonardo da Vinci: Corpus of the Anatomical Studies in the Collection of Her Majesty, the Queen, at Windsor Castle. New York: Harcourt Brace Javonovich, 1978-1980. MCMURRICH, J. P. Leonardo da Vinci, the Anatomist. Baltimore,

MD: Williams & Wilkins, 1930. 9. O’MALLEY, C. D., AND J. B. DE C. M. SAUNDERS. Leonardo da Vinci on the Human Body. New York: Schuman, 1952. 10. R~SCH, F. Observationes anatomicae. Observatio XV. In: Opera Chirurgica. Amsterdam: JanssonioOmnia Anatomico-Medico Waesbergios, 1721. 0. C. L., A. FONAHN, AND H. HOPSTOCK. Leonardo 11. VANGENSTEN, da Vinci: Quaderni d’Anatomie II. Christiana: Casa Editrice Jacob Dybwab, 1912.


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