nevertheless, the arteriae rectee (subsequently called art. rect. verse) were completely injected. He gave figures "drawn as accurately as possible

Transcription

1 THE COURSE OF THE BLOOD OF THE RENAL ARTERY. BY J. N. LANGLEY. (From the Physiological Laboratory, Cambridge.) THERE are many accounts of the blood flow through the kidney. A few only need here be mentioned. Bowman in 1842 described the renal artery as conveying a small quantity of blood direct to the capsule, to the surrounding fat and to the coats of the larger vessels. Except for this small quantity, he considered that the blood conveyed by the renal artery passed through the glomeruli. Virchow in 1857 described the arteries of the boundary layer of the human kidney as giving off small arteries to the medulla, the arteries soon breaking up into a bundle of vessels. In one case of amyloid degeneration of the glomeruli, he stated that the injection mass did not pass through the glomeruli, but that, nevertheless, the arteriae rectee (subsequently called art. rect. verse) were completely injected. He gave figures "drawn as accurately as possible from injected specimens" showing in the clearest way small arteries passing directly to the medulla. This view of a collateral circulation in the kidney was supported by Ludwig, Heidenhain and others. Virchow had pointed out that it was difficult to follow the arterial branches in a fully injected kidney, and in view of this difficulty Golubev in 1893 used silver nitrate as an injection material, thus allowing arteries and veins to be more easily distinguished. He confirmed the existence of art. rectte verse, in not inconsiderable numbers, and stated that in some cases the afferent artery of a glomerulus gave off, close to the glomerulus, a branch supplying blood direct to the kidney tubules. A diagram of this by-pass to the capillaries of the cortex is given in H. Meyer and G ottlieb's Experimentelle Toxicologie, 6th edit. p. 400, 1922, and well illustrates the control which might be exercised on the glomerular blood flow. It may be also mentioned that K olliker and others described small branches of the cortical arteries as running direct to the capsule, and that some observers have found anastomoses between arteries and veins in the capsule of the kidney (Geberg) and in the boundary layer. The question of direct medullary arteries was taken up by Huber (1907). He macerated thick sections of injected kidneys (rat, guinea-pig, rabbit, dog) and found that in nearly all cases each small artery passing PH. LX. 27

2 412 J. N. LANGLEY. to the medulla could be seen to arise from the efferent vessel of the glomerulus (arteriola recta spuria). In the dog he now and then found true direct arteries, but these formed a very small per cent. of the medullary arteries. Occasionally, particularly in the dog, a branch of a cortical artery appeared to anastomose with capsular arteries. He concluded, as had Bowman, that "practically" all the blood passed through the glomeruli. Gerard (1911) examined serial sections of portions of the kidney (rat, rabbit, man) and came to the conclusion that no direct medullary arteries existed. Recently Traut (1923) has made observations on the kidney of man. He macerated the kidney after injecting it from the ureter with a special mixture, and occasionally found a direct medullary artery, but this was rare for in a whole kidney he found six only. In many investigations on secretion by the kidney tubules, it is essential to know whether any appreciable portion of the blood of the renal artery passes to the tubules without passing through the glomeruli. Past observations show that agreement in this point is not likely to be reached by the method of injecting all the vessels. Agreement as to the rarity of arteriolae rectie verae might no doubt be reached by repetition of the method of maceration, but, so far, this rarity has received very scanty recognition by histologists and the maceration method has not been applied to other disputed questions of the kidney circulation. The following method is simple and gives, I think, decisive results on most, if not on all, the questions. The kidney immediately after death is washed out from the renal artery with warm Ringer's fluid to which a drop or two of amyl nitrite is added. A 10 p.c. suspension of rice starch grains in similar warm Ringer's fluid is then injected. The artery is tied, and the kidney placed in formaline (10 p.c.) for a day, and for a day in 50 p.c. alcohol. A piece is cut out of the centre parallel to the medullary rays, soaked in gum and thick sections cut frozen. The rest is cut into slides about 1 mm. thick. The sections and slices are placed in an aqueous solution of iodine dissolved in potassium iodide which quickly stains the arteries black the rest of the tissue brown. If it is required to examine without delay, the sections and slices are placed for 5 to 10 minutes in acetone or absolute alcohol, and as soon as the brown stain has become light-yellow the sections (if necessary further dehydrated) are cleared in clove oil, passed through xylol, mounted in balsam, and examined under the microscope; the slices are transferred to water and examined with a lens. If it is not required to examine at once, it is better to put the sections

3 KIDNEY BLOOD FLOW. 413 and slices in water, until the brown or yellow stain has disappeared; this, according to the duration of stay in iodine, may be any time from an hour to a day. The arteries are then a deep black on a colourless background. When mounted they decolorise in two to six days but they can be re-stained at any time. Sections dried on the slide do not decolorise, they show the position of the arteries, but are useless for microscopic examination. Slides dehydrated and mounted in balsam without a cover slip may last for a month or two. Slices stained with an alcoholic solution of iodine, partially decolorised in alcohol and cleared in clove oil make, when freshly prepared, effective preparations for low power magnification (cf. Fig. 2). I have examined sections and slices of a number of kidneys of the rabbit and one or two of the cat, dog and guinea-pig. The fat tissue in the hilum and around the kidney was generally removed before cutting sections and examined separately. We may consider first the blood of the renal vessels which do not pass to the capillaries of the kidney tubules. In arterial injections, all the arteries of the tissues of the hilum and of the upper half of the ureter are injected. The injection of the capsule and of the fat around the kidney varied and was never complete; the variation may have been due to differences in injection pressure, but the fat no doubt receives blood from other sources than the renal artery. The renal artery supply to the capsule and fat is peculiar. At wide intervals an interlobular artery runs through the cortex with little or no decrease in size and arriving at the surface sends a branch or two at once to the capsule (cf. Fig. 7), and then runs outward, dividing and supplying a considerable mass of fat. So far as I have seen there are only six to eight of these in the whole kidney. In their proximal course they commonly give off arteries to glomeruli. The best way to find them is to turn back the fat gently from the middle of the convex surface of the kidney, flooding with iodine as the fat is separated. The arteries are then seen issuing from the kidney, and thin slices containing them may be cut and treated for microscopic examination. In the two injections made from the renal vein, the veins of the hilum tissue and of the ureter were well injected and one or two small capsular veins. The arteries and veins mentioned above are all small and blood which passes through them can only be a very small proportion of that of the renal vein. On naked eye examination of the mounted sections and slices from which the staining of the tubules has been removed by water, it is seen that whilst the arteries of the boundary layer, the interlobullar arteries 27-2

4 414 J. N. LANGLEY. and the arteries to the glomeruli are dense black, there is hardly a trace of colour in the medulla. The usual appearance is that of Fig. 1. In this at a there is one small injected vessel running into the medulla, and one only. In a good many sections there are none, but there may be two; the most I have seen is three. Fig.. Fig. 2 Fig. 1. Cortical (interlobular) arteries. At a a small direct artery, at b a simall artery of the hilum system. Fig. 2. Boundary layer artery giving off interlobular arteries and these giving off afferent~ glomerular arteries. As a rule the whole course of a direct medullary artery cannot be seen unless the section is thick. The uxsual appearance is shown i Fig. 3 (which is a of Fig. 1 more magnified) and in Fig. 4. Thus usually, to make sure of their origin and courseseveral sectionse must be examined. They usually The whole course can however be seen in thick sections. arise direct from a large artery. I have only seen one instance of a direct medullary artery arising from the afferent artery of a glomerulus. This is shown in Fig. 6. Besides these injected arteries there are sometimes single small injected vessels in various positions in the medulla extending for i to i its length. When they occur there are a few grains of starch to be

5 KIDNEY BLOOD FLOW. 415 Figs Figs. 3 and 4. Arterim rect*s vern as ordinarily seen in sections. Fig. 3 is a of Fig. 1, the artery arises from a small artery in the connective tissue surrounding a larger artery, it divides into three branches, not distinct in the reproduction. Fig. 6. Thick section. Art. rect. ver. arising from an artery giving off two branches each ending in a glomerulus. Fig. 5. Part of injected interlobular artery, each branch ending in a glomerulus, to show that if there were side branches they would be visible. Fig. 7. Interlobular artery (perforating artery) running to the surface of the cortex, sending a branch on each side to the capsule; it continued on into the fat and there supplied a considerable mass of fat tissue.

6 416 J. N. LANGLEY. seen here and there in most of the capillaries. They are caused I think by the smaller starch grains passing into the capillaries under high pressure of injection and accumulating in one or other blocked capillary. But if every medullary injected vessel were a small artery, the amount of blood passing through them would be infinitesimal compared with that passing through the glomeruli. The peripheral part of many of the interlobular arteries and of the glomeruli arising frem them are included in a rather thick section and it is obvious that the afferent glomerular artery gives off no branches conveying blood directly to the capillaries of the tubules. Since the afferent arteries are at different levels it is difficult to obtain a photograph showing how certainly the small arteries can be traced. But Fig. 5 will perhaps be sufficient to indicate that if there were a direct branch it could be easily seen. In the boundary layer the afferent glomerular arteries are much more irregular than they are peripherally, some of them are short, some, especially in the dog, are long, but in a sufficiently thick section it can be seen that, with the rare eexceptions mentioned above, every branch of an artery ends in a glomerulus. The most convincing specimens, both as regards direct arteries to the medulla and direct arteries to the cortex are the slices of kidiey, stained with alcoholic solution of iodine, partly decolorised, cleared in clove oil and examined under a low power of a stereoscopic microscope. These show the manner in which a number of interlobular arteries arise from an artery at different levels in the boundary layer, the numerous afferent glomerular arteries which in the lower part of the cortex run towards the medulla and the irregular course and,... length of these. They show also that in the deeper cortical region it is not infrequent for an afferent glomerular artery to divide, each branch ending in a glomerulus and that this sometimes occurs in the more - superficial region. Occasionally the branching of the artery occurs close to the glomerulus; in a section, one of these branches would probably be cut, and it is possible that the direct artery to the capillaries described by f Golubev was of this kind. Fig. 2 is taken from a slice treated as just described. In the specimen every arterial branch could be followed, under the stereoscopic micro- - scope, to a glomerulus. Fig. 8 is a sketch of part of an " interlobular artery kindly drawn for me by Dr J arisch from a similar specimen. Ei. 8,.5. -.

7 KIDNEY BLOOD FLOW. The results I think show that in the rabbit, cat and dog there are no direct arteries to the cortical capillaries and that so far as there are direct anastomoses between arteries and veins the connecting vessels are of capillary size. I agree with Huber and Traut that the number of small arteries running direct to the medulla is trivial though these arteries are not so rare as they describe. In the guinea-pig, the glomeruli are very close together and I have not examined them in much detail, but, so far as I have seen, the arterial connexions are the same as in the rabbit. On the basis of embryological investigation Traut regards the rare direct medullary arteries as arising from atrophied glomeruli. There are some features of these arteries which lead me to think that most of them do not belong to the circulation of the kidney tubules but to the blood supply of the renal vessels and of the tissues accompanying them. In Fig. 2 it will be seen that the small direct medullary artery is not in the position described for the arteriolae rectee verae, but arises from a small artery in the connective tissue sheath of a relatively large artery. In Fig. 1 there is a small artery at b in the connective tissue of the hilum. An artery in this position not infrequently (in proportion to the total number of direct arteries) sends a branch which curves into the medulla at the base of the papilla, and divides in two or more small branches running towards the apex of the papilla. The renal vein (rabbit) was only injected twice. The interlobular veins and numerous medullary veins were well injected; from the interlobular veins the starch penetrated a short way into the capillaries joining it, but no other part of the kidney substance was injected. 417 SUMMARY. The distribution of the branches of the renal artery can be readily determined by injecting it with a suspension of rice starch grains and staining sections and slices with iodine. The renal artery supplies blood, as originally described by B owm an, to the tissues of the hilum, the capsule and the surrounding fat. The supply to the capsule and the surrounding fat appears however to be partial and variable. The supply is by six or eight interlobular arteries which run through the cortex with little or no decrease in size. The renal artery also supplies blood to the ureter. The renal vein receives blood from the same areas. The cross-section of all the arteries which do not run to the kidney tubules is very small compared with that of the interlobular arteries

8 418 J. N. LANGLEY. but it is conceivable that in certain conditions the quantity of blood passing by them to the renal vein is not negligible. No direct branches to the capillaries of the kidney tubes are given off by the afferent glomerular arteries. The direct arterial branches (arteriolae rects verse) to the medulla are less infrequent than are described by Hu ber and by T raut, but they are so rare and so small that they are certainly negligible in physiological investigations and they cannot be regarded as affording collateral circulation. It is suggested that in origin most of them are not part of the system of vessels supplying the kidney tubules, but are aberrant parts of the vessels supplying the large arteries and veins. The micro-photographs were taken by my laboratory assistant Mr Freeman. They are of the kidney of the rabbit; and of specimens injected from the renal artery. REFERENCES. Bowman. Trans. Roy. Soc Virchow. Virchow's Arch. 12. p Golubev. Intern. J. Anat. and Physiol. 10. p Huber. Amer. J. of Anat. 6. p Gerard. J. de l'anat. et de la Physiol. 47. p Traut. Contributions to Embryology, Carnegie Institute of Washington. Views held at different times with summaries of previous work are given by Ludwig (Stricker's Hdb. d. Gewebelehre, translated by Power, 2. p ), Heidenhain (Hermann's Hdb. d. Physiol. 5. Pt. 1. p ), v. Ebner (KElliker's Hdb. d. Gewebelehre, 6th edit. 3. p ), and Gerard (op. cit. supra).