Generally, the arteries run radially from the periphery towards. study though recent work has shown that the intercostal muscles in the

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1 THE ARTERIAL BLOOD SUPPLY TO THE CAT DIAPHRAGM WITH A NOTE ON THE VENOUS DRAINAGE. By T. J. BIscOE * and ANNE BuCKNELL.t From the War Department, Chemical Defence Experimental Establishment, Porton Down, Near Salisbury, Wilts. (Received for publication 2nd July 1962) In fifty-three cats the arterial blood supply to the diaphragm was studied and some observations made on the venous drainage. The arteries arise from the 8th to 13th intercostal arteries, the internal mammary arteries and from branches of the abdominal aorta. Rarely there are direct branches from both the thoracic and the abdominal aorta. There are considerable variations in the pattern of supply. The veins drain into tributaries of the intercostal veins, the internal mammary veins and into the inferior vena cava. THE contraction characteristics of respiratory muscle have received little study though recent work has shown that the intercostal muscles in the upper seven spaces in the cat are fast in character [Biscoe, 1961]. In order to study the characteristics of the diaphragm in vivo an accurate knowledge of the blood supply is required. This paper describes the blood supply and some of the common anomalies in the cat. METHODS The examination was carried out on fifty-three cats which had been used for other experiments. The abdominal aorta was tied below the posterior mesenteric artery. A cannula was tied into the ascending aorta immediately above the aortic valve and the remainder of the vascular tree perfused through it with 0 9 per cent saline. The right atrium had been opened and when the effluent flowing out of it was clear of blood a thick warm suspension of finely divided barium sulphate (Micropaque) was injected under pressure through the aortic cannula until the vessels over the whole surface of the diaphragm were seen to be satisfactorily filled. The animal was then dissected to expose the upper and lower surfaces of the diaphragm, the vessels and their points of origin. RESULTS The Arterial Blood Supply The diaphragm in the cat has a complex blood supply which is summarized Generally, the arteries run radially from the periphery towards in Table I. the central tendon, each usually anastomosing with its neighbouring vessels on either side to form a complex network throughout the muscle substance. They were found to arise from five main sources: 1. The 8th to 13th intercostal arteries on each side. 2. Branches from the internal mammary arteries on each side which supply the diaphragm ventral to the central tendon. * Present address: ARC, Institute of Animal Physiology, Babraham, Cambridge. t Present address: Bedford College, Regents Park, London, N.W.1. 27

2 28 Biscoe and Bucknell 3. Vessels arising from branches of the abdominal aorta or, rarely, from the abdominal aorta direct, which supply the diaphragm dorsal to the central tendon including the crura. 4. Occasionally branches from the thoracic aorta. 5. The arteries from these sources frequently joined an anastomotic artery around the central tendon. As shown in Table I not all branches were present in each animal. The course and distribution of the most commonly occurring arteries are shown diagrammatically in fig. 1. TABLE I.-THE BLOOD SUPPLY TO THE CAT DIAPHRAGM Group Vessel Right Left 1. Intercostal arteries /53 53/53 2. Internal mammary Lateral branch /52 52/52 Medial branch /52 41/52 3. Abdominal aorta. (i) Phrenic branch of cceliac.. 46/53 32/53 (ii) Phrenic branch of adrenolumbar. 47/53 47/53 (iii) Left gastric.... 9/53 (iv) Hepatic branch.... 8/53 (v) Direct branches.... 0/53 5/53 4. Thoracic aorta Direct branches.... 7/53 5/53 Mid-line branches... 2/53 5. Central tendon anastomotic artery Ventral side /53 Dorsal side /53 The vessels are listed in the order in which they are described in the text. The two columns on the right indicate the number of each vessel found on each side of the body out of the total number of animals used. Fifty-three cats were examined except in group 2, the internal mammary artery, where one preparation was inadvertently destroyed. 1. Intercostal Arteries (fig. 1).-There was usually one branch from each of the lower six intercostal arteries as they coursed postero-laterally round the thoracic wall. The branches lie buried deep in the muscle and are not clearly seen from either the anterior or the posterior surface. The upper four branches entered the upper surface of the muscle but the branches from the 12th and 13th intercostal arteries usually emerged below the diaphragm and entered it on the abdominal surface. The arteries were all directed towards the central tendon and in addition to anastomosing with each other the upper three or four anastomosed around the central tendon with vessels from the other sources. Usually the lower two branches only anastomosed with vessels arising in the abdomen. There was little variation in this pattern. 2. Internal Mammary Artery (fig. 1).-This is a branch of the subclavian artery and its course was observed in fifty-two cats. It runs through the

3 Blood Supply to the Cat Diaphragm muscle near the anterior surface. In all cases a large branch from this artery passed postero-laterally into the diaphragm at the level of the 7th or 8th costal cartilage and anastomosed with the vessels ascending from the abdomen and with the 8th, 9th and 10th intercostal arteries. A second branch usually arose from the internal mammary artery as it passed posteriorly to the abdominal wall to anastomoze with the inferior I.M I(1M. FIG. 1.-Diagram to show some of the I.C.8 A arteries supplying the cat diaphragm. C.M. =costal margin; X =xiphoid carti- 9 lage; L.2 = 2nd lumbar vertebra; C.T. =central tendon; V.C. =vena caval opening in the central tendon; Oes.= 10 cesophageal opening; Th.A. =thoracic C A. aorta; Ab.A. =abdominal aorta; S.M. = superior mesenteric artery; C. coeliac axis; Ad. =adrenal gland; I.M. 1, =internal mammary artery; Med., Lat. =medial and lateral branches of the 12 internal mammary artery; I.C.8, 9, 10, etc. = diaphragmatic branches of the 8th, 9th, 10th, etc. intercostal arteries; Ad.L. =adrenolumbar artery; P.A. = phrenic branch of the adrenolumbar 13 L Q artery; P.C. =phrenic branch of the PA X A. coeliac axis; A. =anastomotic artery. d. SAd. epigastric artery [superior epigastric of man, Reighard and Jennings, 1935]. This branch when present supplied the diaphragm arising from the xiphisternum and the immediately adjacent costal cartilages, i.e. medial to the preceding branch. In eleven out of fifty-two cats it was absent on the left side and it was smaller on the left than on the right in sixteen out of the remaining forty-one cats. On the right side it was absent in one out of fifty-two cats and smaller on the right than, on the left in three of the remainder. In one animal in which this left medial branch was absent the right branch supplied a small artery through the hepatic ligament to the liver. 3. Branches of the Abdominal Aorta.-(i) The Phrenic Artery (fig. 1).- This is the first branch of the cceliac axis and arises shortly after the origin of this artery from the aorta. In the animals examined the phrenic artery usually divided into two branches which passed immediately one into each

4 30 Biscoe and Bucknell crus of the diaphragm. They coursed towards the central tendon the left branch passing lateral to the cesophageal opening. In seven out of fifty-three cats the artery was absent. The left branch was absent in fourteen animals and very much smaller than the right branch in twenty-one cats. In seven animals the left branch crossed the tendon and took part in the anastomosis around it, whilst in four cats this branch supplied only the left crus and adjacent muscle. The right branch of the phrenic artery was commonly the larger of the two; in thirty-eight cats it crossed the tendon on the right side of the vena caval opening and took part in the anastomosis. In five others it reached the tendon and its anastomosis but did not cross it. In three animals in which the left branch was absent the phrenic artery was very small and supplied only the right crus and adjacent muscle. The right branch was never found to be smaller than the left branch nor did the phrenic artery ever supply only the left crus. On one occasion two separate phrenic arteries were seen arising from the cceliac axis, both were large and crossed the central tendon. Twice there were two small branches to the left crus instead of one. (ii) A Phrenic Branch of the Adrenolumbar Artery (fig. 1).-Right and left adrenolumbar arteries commonly arose from the aorta at the level of the 2nd or 3rd lumbar vertebra. One supplied a branch to the diaphragm in forty-seven out of fifty-three cats on the right side and the other one to the same number on the left. In two cats there were no branches to the diaphragm from these arteries and in eight cats a supply from one side only. In eight animals there were two branches from the left artery and in six animals two branches from the right. In one of each of these specimens there was no supply from the other side and in three cases the double supply was common to each side. In three cats the left adrenolumbar artery supplied the right as well as the left crus and left diaphragm below and medial to the tendon. There were therefore in the whole series fifty-five phrenic branches on the left side and fifty-three on the right. Twenty-six of those on the left and six of those on the right crossed the central tendon; twenty-one on the left and forty-one on the right supplied the muscle only below the tendon; eight on the left and six on the right were very small reaching just above the arcuate ligaments. (iii) The Left Gastric Artery.-At the ventral border of the cesophageal opening the left gastric artery continued from the lesser curvature of the stomach to supply the diaphragm in nine out of fifty-three cats. This vessel anastomosed with the other arteries arising from the abdominal aorta and with the intercostal arteries; it also joined the anastomotic artery around the tendon when this was present. Usually a large branch crossed the tendon to anastomose with the internal mammary artery. In one cat a sub-division of this left gastric branch passed to the liver. (iv) A Branch from the Hepatic Artery.-This branch was seen in eight out of fifty-three cats. It commenced at the hilum of the liver and usually ran between the right and left lobes but in one animal penetrated the left

5 Blood Supply to the Cat Diaphragm lobe. The artery usually passed to the left of the inferior vena cava (IVC) to join the anastomosis around the tendon on the ventral side. In one cat the artery passed to the right of the IVC to the anastomosis and in another cat it formed an anastomosis with the phrenic artery on the dorsal side of the tendon. In one cat the hepatic branch passed through connective tissue to the sternum and thence dorsally onto the caudal surface of the diaphragm. (v) Direct Branches from the Abdominal Aorta.-These were seen in only five cats all supplying the left side. When these branches were present the other vessels were smaller or absent. Three of the vessels arose at the same level as the cceliac axis and two at the level of the anterior mesenteric artery. One of the former arose in the mid-line, the others all on the lateral side. In two of the cats in this group there was no phrenic branch of the left adrenolumbar artery and it was very small in the other three. In one of the former and two of the latter there was no left branch of the phrenic artery from the coeliac axis. 4. Direct Branches from the Thoracic Aorta.-These were also uncommon and were seen in eleven cats. The most striking variations were found in this group. There were seven branches on the right side, five on the left and two in the mid-line. In one cat all three vessels occurred. The arteries usually arose just above the diaphragm at the level of the 1st or 2nd lumbar vertebra. Typically the branch would pass laterally from the aorta under the medial arcuate ligament curving ventrally to the caudal surface of the diaphragm. In three cats the arteries on the right also supplied the adrenal gland, for there was no adrenolumbar artery. Two of the arteries on the right side and one of the two arising in the mid-line did not pass below the diaphragm. The second branch arising in the mid-line passed below the median arcuate ligament to supply the diaphragm and left adrenal gland. Other vessels to the diaphragm were smaller than usual when these arteries were present. The phrenic branch of the coeliac was present in all but one, though its branch to the left side was always small and was absent in three animals. In eight cats the phrenic branch of the adrenolumbar artery was absent on the side supplied by the thoracic aorta and in one cat it was very much smaller than usual. 5. The Anastomotic Artery around the Central Tendon (fig. 1).-The arteries invariably anastomosed in the vicinity of the tendon but there was commonly a well-defined vessel running around the ventral edge of the central tendon connecting the other arteries, viz. internal mammary, phrenic branch of the coeliac, etc. This vessel was present in forty-five of the cats and continued round the dorsal side of the central tendon in fourteen of these. It was absent in eight cats though the usual anastomotic vessels were present in the substance of the diaphragm. 31

6 32 Biscoe and Bucknell The Venous Drainage This could not be easily studied in these preparations because of the density of the arteries and no figures are available about the distribution of veins. However, there appeared to be three major groups of veins: 1. Veins running with the branches of the intercostal arteries to join the intercostal veins. 2. Tributaries of the internal mammary veins. 3. Veins joining the inferior vena cava either directly, or indirectly through a vessel on each side which usually runs on the posterior surface of the lateral extensions of the diaphragm. DISCUSSION The account of the blood supply to the diaphragm of the cat given by Mivart [1881] is inaccurate. He describes a superior phrenic branch of the internal mammary artery "which passes backwards to the diaphragm between the lung root and the pericardium". Such a vessel was not seen in this series. He also describes an inferior phrenic which is a branch of the abdominal aorta, is very small and "goes to the hinder surface of the diaphragm". In five of the cats a vessel which approximately fitted this description was seen. Also there is no mention in this book by Mivart [1881] of a supply from the intercostal, cceliac or adrenolumbar arteries. According to Reighard and Jennings [1935], the blood supply to the diaphragm is derived from the internal mammary arteries, and a phrenic branch of the cceliac or a phrenic branch of the adrenolumbar artery. In this series the internal mammary arteries were fairly constant in their distribution. However, in only thirteen out of the fifty-three cats was the blood supply to the diaphragm dorsal to the tendon as simple as that described above. In these thirteen, only phrenic branches of the coeliac axis and of the adrenolumbar arteries were present. All the other forty cats had at least one "anomaly" varying from the simple duplication of one branch of the adrenolumbar artery to the uncommon branches originating direct from the thoracic aorta. There were in fact ninety-six " anomalies " in these forty cats. Commonly when one artery was large others were smaller or absent. For example, the right branch of the phrenic artery from the cceliac was usually larger than the left whilst the phrenic branch of the left adrenolumbar artery was usually larger than the corresponding branch of the right adrenolumbar. The pericardiacophrenic artery found in man was not seen in any of the cats in this series. There are considerable variations in the blood supply to the diaphragm but an awareness of the common anomalies reviewed here will need to be borne in mind in any attempt to use this muscle for experimental purposes. If the contraction characteristics are to be studied in vivo the blood supply

7 Blood Supply to the Cat Diaphragm to the muscle must be preserved. Also if the cat diaphragm is ever to be used as an isolated muscle preparation it would need to be perfused as adequate oxygenation could not be maintained by surface diffusion from the medium. Drugs have been injected into the isolated rat diaphragm through a cannula in the inferior vena cava by Burgen, Dickens and Zatman [1949]. Brownlee and Straughan [1957] used a similar route to perfuse a sector of the diaphragm in the rat when they studied the release of acetylcholine on stimulation of the motor nerve. They collected the effluent from the cut arteries. To perfuse the whole cat diaphragm via the venous route cannule in both the superior and inferior vene cavse would be required. The former to include the internal mammary veins, the latter the veins from other sources. The whole of the effluent could be collected from the arteries though this would be difficult for there are many of them, and collection from the aorta would include other muscles. Also it is not clear how important valves in the veins would be in interfering with perfusion by this route. Perfusion from the arterial side could be accomplished through a cannula in the ascending aorta with the abdominal aorta tied below the renal arteries. Collection of the perfusate from the whole diaphragm only would again be very difficult. A compromise would have to be made, either to include some of the chest-wall perfusate or to exclude that coming from the small tributaries of the intercostal veins for these could hardly be cannulated separately. Collection of perfusate may not be important in some studies but, if perfusate from the diaphragm only uncontaminated by other sources is required collection from specific well-defined areas would be the simplest solution. For example from one artery on venous perfusion or one vein on arterial perfusion. Some of the vessels are large enough for this to be possible. Alternatively one segment of the diaphragm could be perfused alone; the ventral portion on one side is the most obvious choice for here both the internal mammary artery and the vein could probably be cannulated. ACKNOWLEDGMENT We are grateful to Mr. B. Aldous for unfailing technical assistance. 33 REFERENCES BIsCOE, T. J. (1961). "Some properties of intercostal muscle in the cat"', J. ishysiol. 159, 31-32P. BROWNLEE, G. and STRAUGHAN, D. W. (1957). "Motor nerve stimullation and acetylcholine release in the perfused rat phrenic nerve diaphragm preparation", J. Ph1ysiol. 136, 6P. BURGEN, A. S. V., DICKENS, F. and ZATMAN, L. J. (1949). "The action of botulinium toxin on the neuromuscular junction", J. Physiol. 109, MIVART, ST. G. (1881). The Cat. An Introduction to the Study of Backboned Animals especially Mammals, pp. 209, 211. London: John Murray. REIGHARD, J. and JENNINGS, H. S. (1935). Anatomy of the Cat, 3rd Ed., pp. 283, 292, 304. New York: Henry Holt. VOL. XLVIII, No