Efferent Arterioles in the Cortex of the Rat Kidney ANDREW P. EVAN AND WILLIAM G. DAIL, JR. Department of Anatomy, The University of New Mexico School of Medzcine, Albuquerque, New Mexico 871 31
ABSTRACT Although a number of morphological studies have investigated the vascular system of the rat kidney, minimal data are available on the detailed anatomy of the efferent arterioles located throughout the cortex of the kidney. In the present study, the renal vascular system was filled with Microfil and the various efferent arteriole patterns were examined extensively. The efferent vessels of the entire cortex appear to form three major patterns which in turn divided the cortex into three separate regions: the outer, middle and inner cortex. The efferent arterioles of the outer cortex leave the glomerulus and run perpendicular to the kidney capsule. However, as the efferent arterioles ascend, they may show three variations in the way they branch: (la) the efferent arteriole does not branch until directly beneath the capsule, (lb) the efferent vessel begins to divide into its major branches 100-200 pm below the surface of the kidney and (lc) the efferent vessel has only a short course before giving off many side branches. In the middle corrical area, the branches of the efferent arteriole run lateral to the glomerulus. However, the efferent arterioles of the inner cortex have a few branches which run lateral to the glomerulus while most of them descend into the medulla as vasa rectae. The unique morphological features of the efferent arterioles of the outer cortex are of particular interest in light of the functional data which suggests that the reabsorption of fluid by peritubular capillaries may indeed regulate the rate of net tubular sodium reabsorption.
The vascular system of the kidney has been investigated for many years employing a variety of techniques (Bowmen, 1842; Mollendorff, '30; Trueta et al., '47). The purpose of many of these studies was to understand the flow of blood through the kidney, however the possible functional importance of the branching pattern of the efferent arterioles of the glomerulus was not fully appreciated. From these earlier studies it was thought that only two patterns of efferent arterioles existed; one for the cortical nephrons and another for the juxtamedullary nephrons. With newer techniques and improved filling compounds such as Microfil, it has been shown that many different efferent arteriole patterns are present in the dog and human kidney (Ljungquist and Lagergren, '62; Moffat and Fourman, '63; Beeuwkes, '71). Although the rat is the most commonly used animal for studies of renal function, its renal vasculature has not been studied in detail. The purpose of the present investigation is to reexamine the vasculature of the rat kidANAT. REC., 187: 135-146.
ney with more refined casting techniques. Emphasis has been placed on the efferent arterioles and their branches of the outer cortex in view of their presumed importance in regulating tubular reabsorption. MATERIALS AND METHODS
Twenty-four adult male rats ranging in weight from 228-275 gm were used. The animals were anesthetized with Inactin and secured to a dissection board. The left external jugular vein was exposed and cannulated with polyethylene tubing (PE90) for administration of sodium Heparin. Five minutes later an abdominal incision was made to expose the abdominal aorta. A ligature was quickly placed around the abdominal aorta just below the diaphragm and another just proximal to the origin of the common iliac vessels. The aorta was cannulated between the ligatures with PE90. The renal veins were incised immediately and the injection media Microfd MV-112 Received July 23,'76.Accepted Sept. 9,'76.
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(Canton Biomedical Products, Boulder, Colorado) was infused into the renal vascular system at a pressure of 25-125 mm Hg. Different levels of vascular filling were obtained by (1) just filling the outer cortical vessels or (2) perfusing the kidney until the Microfil was seen flowing out of the renal vein. The first method filled only a few outer cortical efferent arterioles while method 2 generally filled a majority of the vascular system of the kidney. The more completely the vascular system was filled, the more difficult i t became to visualize single efferent systems. At the desired extent of filling, the renal artery and vein were clamped at the hilus and the Microfil was allowed to polymerize for one hour. Subsequently, the kidneys were removed, sliced perpendicular to their long axis, fixed overnight in 10% buffered formalin and slowly dehydrated through a series of graded ethanols (24 hours in each alcohol solution). The kidneys were then transferred from absolute ethanol to methyl salicylate (oil of wintergreen) for clearing and storage. The vascular casts were viewed with a Wild MT-5 Stereomicroscope and photographed on Polaroid 55 film.
has a depth of one or two glomeruli, will be referred to as the outer cortex. In this region the efferent vessel leaves the glomerulus and runs perpendicular to the kidney capsule (figs. 2-4). The diameter of the proximal end of the efferent arteriole is always smaller than its corresponding afferent arteriole. However, as the efferent vessel rises to the capsule, its diameter may increase by threefold. As the efferent vessel approaches the capsule, it may show three variations in the way it branches to form peritubular capillaries. In the first variation ( l a ) the efferent arteriole does not branch until directly beneath the capsule (fig. 2). The location at which its main branches (usually five) arise is termed a “welling point” (Steinhausen, ’63). Only occasionally could a small side branch be seen coming off of the efferent vessel before it reaches the capsule. Approximately 40% of all the outer cortical glomeruli had this branching pattern. In the second variation (Ib) the efferent vessel begins to divide into two or three main branches about 100-200 p m below the surface of the kidney (fig. 3 ) . Thus the “welling point” is well below the capsule RESULTS of the kidney (arrow in fig. 3). The two or Since considerable work has been done three main branches continue to rise describing the order of branching of the towards the capsule where they form nuarteries of the kidney to the level of the merous branches. Approximately 30% of glomerulus, our description will start at the glomeruli have this kind of branching. In the final pattern ( l c ) the efferent vesthe glomerulus and follow the efferent arteriole at various levels of the cortex. sel has a short course before giving off Branching of the efferent vessels into peri- many side branches (fig. 4). Several of these tubular capillaries in the cortex appear to branches may reach the surface of the form three major patterns: (1) efferent kidney. Approximately 30% of the outer vessels with branches which rise directly cortical glomeruli show this third variation. to the kidney capsule, (2) those with These three variations are randomly disbranches which run lateral to the glomeru- tributed throughout the outer cortex. lus and ( 3 ) efferent arterioles which have The welling points of l a and I b efferent some branches which run lateral while vessels may be seen from the surface of others descend into the medulla (figs. 1 , 8). the kidney (figs. 5a-c). A definite welling Each of these patterns is localized to a par- point for the type l c efferent arteriole canticular region of the cortex. The first pat- not be seen because of the irregular pattern is found in the outer cortex, the second tern of branching. In the type l a efferent in the middle cortical region and the third arterioles, the five to six main branches in the inner cortex. radiate from a single point, forming the so-called “star” arrangement (figs. 5a,b). Outer cortical efferents (subcapsular) The main branches divide several more The efferent arteriole pattern described times before they coalesce and join the vein this section is limited to those glomeruli nous return. In type l b pattern (figs. 5a,c) which lie just beneath the capsule of the however, the true welling point is the point kidney. This region of the kidney, which at which the main vessel divides into two
EFFERENT VESSELS OF KIDNEY
large branches (arrow in fig. 3). The further division of these two branches, some of which communicate, may have the appearance of welling points near the kidney capsule. Mid cortical efferents Approximately 90% of all glomeruli in this region of the cortex have the same pattern of branches of efferent vessels. The arteriole arises from the lateral side of the glomerulus and immediately divides into a network of peritubular capillaries close to the glomeruli (fig. 6). Individual peritubular capillaries may have a larger diameter than the parent efferent arteriole. The complexity of the network makes it difficult to follow individual capillaries. The only other kind of efferent vascular pattern noted i n the midcortex was one identical to the type I c outer cortical efferent system with the exception that none of the branches reached the kidney capsule. Only glomeruli found directly beneath the outer cortical glomeruli had this efferent arrangement.
lnner cortical efferent patterm (jux t amedullary) At the cortico-medullary junction, the efferent patterns change considerably when compared to the other two cortical regions. The efferent vessel descends into the outer medulla and divides many times to form the vasa rectae (fig 7). The rest of the course of the vasa rectae through the outer and inner medulla has been described by other workers and will not be dealt with here. Unlike efferent vessels of the outer cortex the efferent arteriole in the juxtamedullary zone has the same diameter as the afferent arteriole. The efferent arteriole and vasa recta maintain this diameter as they give off many small capillaries through the medulla. In many juxtamedullary glomeruli a small branch arises from the main stem of the efferent arteriole (arrow in fig. 7 ) and coursed laterally to form a peritubular network similar to that seen for midcortical glomeruli. When this small side branch was absent, the efferent arteriole appeared as one main stem directed toward the medulla. DISCUSSION
The results of the present study show
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three distinct efferent vascular patterns in the cortex of the rat kidney (fig. 8). The first group of vessels always rises to the capsule of the kidney and is referred to as the outer cortical or subcapsular efferents. In the second group the branches of the efferent vessels are located lateral to and in close approximation to the glomerulus. These vessels are designated midcortical efferents. The last group is located in the inner cortex or juxtamedullary area and have one vessel that goes to the medulla as the vasa rectae and another that remains lateral to the glomerulus. These findings differ from other studies (Ljungquist and Lagergren, '62; Moffat and Fourman, '63) which have described only two zones in the cortex. Failure of previous studies to identify a third type of vascular pattern is probably due to their emphasis on the juxtamedullary area of the kidney rather than the outer cortex. Although we cannot directly determine the functional significance of this organization, it is reasonable to assume that it may reflect a varied relationship between capillaries and tubules at different levels in the cortex. In support of the concept, Beeuwkes and Bonventre ('75) have shown that in the dog kidney, efferent vessels in the outer cortex are closely associated with their own nephron, while in the juxtamedullary area, efferent vessels are frequently related to neighboring nephrons. In a limited study, Steinhausen ('63) has shown that the peritubular capillaries in the outer cortex of the rat kidney are also closely related to their own nephron. The efferent arterioles found in the outer cortex have several unique morphological features. It has been noted by other workers that the diameter of the efferent arteriole at the glomerulus is smaller than the afferent vessel. In addition we have observed that the efferent vessel gradually increases in size until it reaches the welling point. It is known from transmission electron microscopic studies that the ultrastructure of the cortical efferent arteriole is that of a typical arteriole (Fourman and Moffat, '71). It is interesting to speculate that the narrowed end of the efferent arteriole may be themajor site which regulates the vascular resistance of the efferent vessel. This becomes important when one considers that the efferent arteriole is in part
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ANDREW P. EVAN AND WILLIAM G . DAIL, JR
responsible for the regulation of glomerular capillary pressure as well as renal blood flow (Barger and Herd, ’73). Recently it has become apparent that reabsorption of fluid by peritubular capillaries may regulate the rate of net tubular sodium reabsorption (Martino and Earley, ’67; Bung and Orloff, ’68; Brenner et al., ’69; Brenner and Troy, ’71; Brenner and Galla, ’71; Seely, ’73). One factor affecting the rate of capillary reabsorption is the capillary hydrostatic pressure. For example, a low capillary hydrostatic pressure compared to a higher tubular or interstitial hydrostatic pressure would favor reabsorption by peritubular capillaries. The increasing diameter of the efferent arteriole with the consequent lowering of the hydrostatic pressure may favor tubular reabsorption. In support of this idea, Allison et al. (‘72) have shown a distinct fall in the mean hydrostatic pressure along the post-glomerular network. Although there are several reports that indicate that peritubular capillaries control tubular reabsorption, no study has described in any great detail the organization of the capillary network beneath the capsule of the kidney. In the present study we have found that approximately twothirds of the efferent vessels of the outer cortex or subcapsular region divide into a capillary network just beneath the capsule of the kidney. The point at which the main branches arise from the efferent vessel, whether they are capillaries or smaller arterioles, has been termed the welling point. This area is visible on the surface of the kidney. The pattern of branching of the efferent vessel is suggestive of a “star” (Steinhausen, ’63). However, we found that only about 50% of the networks on the surface of the kidney have the “star” arrangement. The remaining patterns of the surface of the kidney do not have a star arrangement. The efferent vessel of these glomeruli rises to within 100 p m of the surface of the kidney and divides into two large branches each of which forms a peritubular network of capillaries. Therefore, for this efferent pattern the true welling point is not on the surface of the kidney and consequently is not accessible for micropuncture studies. From these studies, it is apparent that caution must be exer-
cised in sampling blood from the peritubular capillary system. Since there are several extensive studies of the vasa recta, our comments will be limited to the number of efferent vessels which arise from the juxtamedullary nephron. In the present study, a majority of these glomeruli have two branches, One branch remains in the cortical region, while the other descends to the medulla as the vasa recta. Conflicting reports in the literature on the pattern of efferent arterioles in the juxtamedullary area (Gksslen, ’34; Boenig, ’36; Ljungquist and Lagergren, ’62; Moffat and Fourman, ’63) may be due to filling defects which prevent all the branches of a n efferent arteriole from being visualized. ACKNOWLEDGMENTS
We would like to thank Pat Carlton and Judy DeLongo for their excellent technical help, and Paul Goodman for the art work. LITERATURE CITED Allison, M. E. M., E. Lipham and C. W. Gottschalk 1972 Hydrostatic pressure in the rat kidney. h e r . J. Physiol., 223: 975-983. Barger, A. C., and J. A. Herd 1973 Renal vascular anatomy and distribution of blood flow. In: Handbook of Physiology. Section 8. J. Orloff and R. W. Berliner, eds. American Physiological Society, Washington, D.C., pp. 249-313. Beeuwkes, R. 1971 Efferent vascular patterns and early vascular-tubular relations in the dog kidney. Amer. J. Physiol., 221; 1361-1374. Beeuwkes, R., and J. V . Bonventre 1975 Tubular organization and vascular-tubular relations in the dog kidney. h e r . J. Physiol., 229: 695714. Boenig, H. 1936 Beitrage zur Kenntnis der Vasa efferentiain dermenschlichen Niene. 2.mikranat. Forsch., 39: 105-115. Bowman, W. 1842 On the structure and use of the Malpighian bodies of the kidney with observations on the circulation through that gland. Phil. Trans. R. Soc. Ser., 1 : 57-80. Brenner, B. M., K. H. Falchuk, R. I. Keimowitz and R. W. Berliner 1969 The relationships between peritubular capillary protein concentration and fluid reabsorption by the proximal tubule. J. Clin. Invest., 48: 1519-1531. Brenner, B. M., and J. H. Galla 1971 Influence of post-glomerular hematocrit and protein concentration in rat nephron fluid transfer. Amer. J. Physiol., 220: 148-161. Brenner, B. M., and J. L. Troy 1971 Post-glomerular vascular protein concentrations. Evidence for a causal role in governing fluid reabsorption and glomerulotubular balance by the renal proximal tubule. J. Clin. Invest., 50: 336349.
EFFERENT VESSELS OF KIDNEY Burg, M. B., and J. Orloff 1968 Control of fluid absorption in the renal proximal tubule. J. Clin. Invest., 47: 2016-2024. Fourman, J., and D. B. Moffat 1971 The Blood Vessels of the Kidney. J . Fourman and D. B. Moffat, eds. Blackwell Scientific Publication, Oxford, pp. 90-114. Gansslen, M. 1934 Der feinere Gefassaufbau gesunder und Kranker menschlichen Nieren. Ergebn. inn. med. Kinderheilk, 47: 275420. Ljungquist, A., and C. Lagergren 1962 Normal intrarenal arterial pattern in adult and aging human kidney. J. Anat., 96: 285300. Martino, J. A., and L. E. Earley 1967 Demonstration of a role of physical factors as determinants of the natriuretic response to volume expansion. J. Clin. Invest., 46: 1953-1978. Moffat, D. B., and J . Fourman 1963 The vascular pattern of rat kidney. J. Anat., 97: 543-553.
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Mollendorff, W. von 1930 Der Erkretion-apparat i n Handblich der mikroscopischen Anatomie des Menschen 7, Berlin, Springer Verlag, pp. 107130. Seely, J. K. 1973 Effects of peritubular oncotic pressure on rat proximal tubule electrical resistance. Kid. Int., 4: 2 8 4 1 . Smith, J. P. 1956 Anatomical features of the human renal glomerular efferent vessel. J. Anat., 90: 290-292. Steinhausen, M . 1963 Eine Methode zur differenzierung proximalen und distalen tubuli der Nierenrinde von Ratten in vivo und ihre Anwendung zur Bestimmung tubularen Stromungsgeschwindigkeiten. Pfluger Arch. ges Physiol., 277: 2 3 4 5 . b e t a , J., A. E. Barclay, P.M. Daniel, K. J. Franklin and M. M. L. Prichard 1947 Studies of the Renal Circulation. Oxford, Blackwell.
PLATE I EXPLANATION OF FIGURES
140
1
A low power view of the cortex of the rat kidney which has been injected with Microfil. This micrograph illustrates the three regions of the cortex which were studied: 0. outer, M, middle; I, inner. IL, interlobular artery. X 50.
2
A glomerulus in the outer cortex which has the l a type of efferent pattern (enlargement of an area i n fig. 1). Note the large diameter of the afferent arteriole (AA). The efferent arteriole (EA) is thin and branches at the capsule (arrows). X 200.
3
Efferent vessels of this glomerulus in the outer cortex have a type l b pattern. The efferent arteriole divides into two main branches well below the capsule. The welling point is indicated by the arrow. X 200.
4
Outer cortical glomerulus with the type l c efferent pattern. This pattern is characterized by an efferent vessel which divides into numerous branches beneath the capsule of the kidney. In this pattern there is not an identifiable welling point. X 200.
EFFERENT VESSELS OF KIDNEY Andrew P. Evan and William G. Dail, Jr
PLATE 1
141
PLATE 2 EXPLANATION O F FIGURES
142
5a-c
Branching patterns of efferent arterioles which lie directly beneath the capsule. The type l a pattern (fig. 2 ) resembles a “star” and has a distinct welling point (arrow). A more complex pattern arises from the two main branches of the type l b efferent arteriole (fig. 3). Figure 5b is a drawing of the “star” arrangement of the type l a efferent pattern and figure 5c illustrates the branching of type l b efferent pattern. 5a X 250; 5b X 250; 5c X 250.
6
In this example of a midcortical glomerulus, the efferent arteriole gives rise to a number of branches which form a complex capillary network lateral to the glomerulus. The branches do not rise to the capsule. x 200.
7
The efferent vessel of juxtamedullary glomeruli may divide immediately into a small cortical (arrow) and a larger medullary (double arrow) branch. The cortical branch forms a capillary bed in the vicinity of the glomerulus while the medullary branch descends into the medulla to form the vasa recta. X 150.
EFFERENT VESSELS OF KIDNEY Andrew P. Evan and William G. Dail, Jr.
PLATE 2
143
PLATE 3 EXPLANATION
8
144
O F FIGURES
Summary diagram of the branching pattern of efferent arterioles of the rat kidney. Three zones of the cortex (outer, middle and inner) may be defined by variations i n the branching pattern. In the outer cortex, the efferent arterioles branch at different levels to form three distinct types of glomerular efferents ( l a , lb, lc).
EFFERENT VESSELS OF KIDNEY Andrew P. Evan and William G. Dail, Jr
PLATE 3
8 145
ABSTRACT Although a number of morphological studies have investigated the vascular system of the rat kidney, minimal data are available on the detailed anatomy of the efferent arterioles located throughout the cortex of the kidney. In the present study, the renal vascular system was filled with Microfil and the various efferent arteriole patterns were examined extensively. The efferent vessels of the entire cortex appear to form three major patterns which in turn divided the cortex into three separate regions: the outer, middle and inner cortex. The efferent arterioles of the outer cortex leave the glomerulus and run perpendicular to the kidney capsule. However, as the efferent arterioles ascend, they may show three variations in the way they branch: (la) the efferent arteriole does not branch until directly beneath the capsule, (lb) the efferent vessel begins to divide into its major branches 100-200 pm below the surface of the kidney and (lc) the efferent vessel has only a short course before giving off many side branches. In the middle corrical area, the branches of the efferent arteriole run lateral to the glomerulus. However, the efferent arterioles of the inner cortex have a few branches which run lateral to the glomerulus while most of them descend into the medulla as vasa rectae. The unique morphological features of the efferent arterioles of the outer cortex are of particular interest in light of the functional data which suggests that the reabsorption of fluid by peritubular capillaries may indeed regulate the rate of net tubular sodium reabsorption.
The vascular system of the kidney has been investigated for many years employing a variety of techniques (Bowmen, 1842; Mollendorff, '30; Trueta et al., '47). The purpose of many of these studies was to understand the flow of blood through the kidney, however the possible functional importance of the branching pattern of the efferent arterioles of the glomerulus was not fully appreciated. From these earlier studies it was thought that only two patterns of efferent arterioles existed; one for the cortical nephrons and another for the juxtamedullary nephrons. With newer techniques and improved filling compounds such as Microfil, it has been shown that many different efferent arteriole patterns are present in the dog and human kidney (Ljungquist and Lagergren, '62; Moffat and Fourman, '63; Beeuwkes, '71). Although the rat is the most commonly used animal for studies of renal function, its renal vasculature has not been studied in detail. The purpose of the present investigation is to reexamine the vasculature of the rat kidANAT. REC., 187: 135-146.
ney with more refined casting techniques. Emphasis has been placed on the efferent arterioles and their branches of the outer cortex in view of their presumed importance in regulating tubular reabsorption. MATERIALS AND METHODS
Twenty-four adult male rats ranging in weight from 228-275 gm were used. The animals were anesthetized with Inactin and secured to a dissection board. The left external jugular vein was exposed and cannulated with polyethylene tubing (PE90) for administration of sodium Heparin. Five minutes later an abdominal incision was made to expose the abdominal aorta. A ligature was quickly placed around the abdominal aorta just below the diaphragm and another just proximal to the origin of the common iliac vessels. The aorta was cannulated between the ligatures with PE90. The renal veins were incised immediately and the injection media Microfd MV-112 Received July 23,'76.Accepted Sept. 9,'76.
135
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(Canton Biomedical Products, Boulder, Colorado) was infused into the renal vascular system at a pressure of 25-125 mm Hg. Different levels of vascular filling were obtained by (1) just filling the outer cortical vessels or (2) perfusing the kidney until the Microfil was seen flowing out of the renal vein. The first method filled only a few outer cortical efferent arterioles while method 2 generally filled a majority of the vascular system of the kidney. The more completely the vascular system was filled, the more difficult i t became to visualize single efferent systems. At the desired extent of filling, the renal artery and vein were clamped at the hilus and the Microfil was allowed to polymerize for one hour. Subsequently, the kidneys were removed, sliced perpendicular to their long axis, fixed overnight in 10% buffered formalin and slowly dehydrated through a series of graded ethanols (24 hours in each alcohol solution). The kidneys were then transferred from absolute ethanol to methyl salicylate (oil of wintergreen) for clearing and storage. The vascular casts were viewed with a Wild MT-5 Stereomicroscope and photographed on Polaroid 55 film.
has a depth of one or two glomeruli, will be referred to as the outer cortex. In this region the efferent vessel leaves the glomerulus and runs perpendicular to the kidney capsule (figs. 2-4). The diameter of the proximal end of the efferent arteriole is always smaller than its corresponding afferent arteriole. However, as the efferent vessel rises to the capsule, its diameter may increase by threefold. As the efferent vessel approaches the capsule, it may show three variations in the way it branches to form peritubular capillaries. In the first variation ( l a ) the efferent arteriole does not branch until directly beneath the capsule (fig. 2). The location at which its main branches (usually five) arise is termed a “welling point” (Steinhausen, ’63). Only occasionally could a small side branch be seen coming off of the efferent vessel before it reaches the capsule. Approximately 40% of all the outer cortical glomeruli had this branching pattern. In the second variation (Ib) the efferent vessel begins to divide into two or three main branches about 100-200 p m below the surface of the kidney (fig. 3 ) . Thus the “welling point” is well below the capsule RESULTS of the kidney (arrow in fig. 3). The two or Since considerable work has been done three main branches continue to rise describing the order of branching of the towards the capsule where they form nuarteries of the kidney to the level of the merous branches. Approximately 30% of glomerulus, our description will start at the glomeruli have this kind of branching. In the final pattern ( l c ) the efferent vesthe glomerulus and follow the efferent arteriole at various levels of the cortex. sel has a short course before giving off Branching of the efferent vessels into peri- many side branches (fig. 4). Several of these tubular capillaries in the cortex appear to branches may reach the surface of the form three major patterns: (1) efferent kidney. Approximately 30% of the outer vessels with branches which rise directly cortical glomeruli show this third variation. to the kidney capsule, (2) those with These three variations are randomly disbranches which run lateral to the glomeru- tributed throughout the outer cortex. lus and ( 3 ) efferent arterioles which have The welling points of l a and I b efferent some branches which run lateral while vessels may be seen from the surface of others descend into the medulla (figs. 1 , 8). the kidney (figs. 5a-c). A definite welling Each of these patterns is localized to a par- point for the type l c efferent arteriole canticular region of the cortex. The first pat- not be seen because of the irregular pattern is found in the outer cortex, the second tern of branching. In the type l a efferent in the middle cortical region and the third arterioles, the five to six main branches in the inner cortex. radiate from a single point, forming the so-called “star” arrangement (figs. 5a,b). Outer cortical efferents (subcapsular) The main branches divide several more The efferent arteriole pattern described times before they coalesce and join the vein this section is limited to those glomeruli nous return. In type l b pattern (figs. 5a,c) which lie just beneath the capsule of the however, the true welling point is the point kidney. This region of the kidney, which at which the main vessel divides into two
EFFERENT VESSELS OF KIDNEY
large branches (arrow in fig. 3). The further division of these two branches, some of which communicate, may have the appearance of welling points near the kidney capsule. Mid cortical efferents Approximately 90% of all glomeruli in this region of the cortex have the same pattern of branches of efferent vessels. The arteriole arises from the lateral side of the glomerulus and immediately divides into a network of peritubular capillaries close to the glomeruli (fig. 6). Individual peritubular capillaries may have a larger diameter than the parent efferent arteriole. The complexity of the network makes it difficult to follow individual capillaries. The only other kind of efferent vascular pattern noted i n the midcortex was one identical to the type I c outer cortical efferent system with the exception that none of the branches reached the kidney capsule. Only glomeruli found directly beneath the outer cortical glomeruli had this efferent arrangement.
lnner cortical efferent patterm (jux t amedullary) At the cortico-medullary junction, the efferent patterns change considerably when compared to the other two cortical regions. The efferent vessel descends into the outer medulla and divides many times to form the vasa rectae (fig 7). The rest of the course of the vasa rectae through the outer and inner medulla has been described by other workers and will not be dealt with here. Unlike efferent vessels of the outer cortex the efferent arteriole in the juxtamedullary zone has the same diameter as the afferent arteriole. The efferent arteriole and vasa recta maintain this diameter as they give off many small capillaries through the medulla. In many juxtamedullary glomeruli a small branch arises from the main stem of the efferent arteriole (arrow in fig. 7 ) and coursed laterally to form a peritubular network similar to that seen for midcortical glomeruli. When this small side branch was absent, the efferent arteriole appeared as one main stem directed toward the medulla. DISCUSSION
The results of the present study show
137
three distinct efferent vascular patterns in the cortex of the rat kidney (fig. 8). The first group of vessels always rises to the capsule of the kidney and is referred to as the outer cortical or subcapsular efferents. In the second group the branches of the efferent vessels are located lateral to and in close approximation to the glomerulus. These vessels are designated midcortical efferents. The last group is located in the inner cortex or juxtamedullary area and have one vessel that goes to the medulla as the vasa rectae and another that remains lateral to the glomerulus. These findings differ from other studies (Ljungquist and Lagergren, '62; Moffat and Fourman, '63) which have described only two zones in the cortex. Failure of previous studies to identify a third type of vascular pattern is probably due to their emphasis on the juxtamedullary area of the kidney rather than the outer cortex. Although we cannot directly determine the functional significance of this organization, it is reasonable to assume that it may reflect a varied relationship between capillaries and tubules at different levels in the cortex. In support of the concept, Beeuwkes and Bonventre ('75) have shown that in the dog kidney, efferent vessels in the outer cortex are closely associated with their own nephron, while in the juxtamedullary area, efferent vessels are frequently related to neighboring nephrons. In a limited study, Steinhausen ('63) has shown that the peritubular capillaries in the outer cortex of the rat kidney are also closely related to their own nephron. The efferent arterioles found in the outer cortex have several unique morphological features. It has been noted by other workers that the diameter of the efferent arteriole at the glomerulus is smaller than the afferent vessel. In addition we have observed that the efferent vessel gradually increases in size until it reaches the welling point. It is known from transmission electron microscopic studies that the ultrastructure of the cortical efferent arteriole is that of a typical arteriole (Fourman and Moffat, '71). It is interesting to speculate that the narrowed end of the efferent arteriole may be themajor site which regulates the vascular resistance of the efferent vessel. This becomes important when one considers that the efferent arteriole is in part
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ANDREW P. EVAN AND WILLIAM G . DAIL, JR
responsible for the regulation of glomerular capillary pressure as well as renal blood flow (Barger and Herd, ’73). Recently it has become apparent that reabsorption of fluid by peritubular capillaries may regulate the rate of net tubular sodium reabsorption (Martino and Earley, ’67; Bung and Orloff, ’68; Brenner et al., ’69; Brenner and Troy, ’71; Brenner and Galla, ’71; Seely, ’73). One factor affecting the rate of capillary reabsorption is the capillary hydrostatic pressure. For example, a low capillary hydrostatic pressure compared to a higher tubular or interstitial hydrostatic pressure would favor reabsorption by peritubular capillaries. The increasing diameter of the efferent arteriole with the consequent lowering of the hydrostatic pressure may favor tubular reabsorption. In support of this idea, Allison et al. (‘72) have shown a distinct fall in the mean hydrostatic pressure along the post-glomerular network. Although there are several reports that indicate that peritubular capillaries control tubular reabsorption, no study has described in any great detail the organization of the capillary network beneath the capsule of the kidney. In the present study we have found that approximately twothirds of the efferent vessels of the outer cortex or subcapsular region divide into a capillary network just beneath the capsule of the kidney. The point at which the main branches arise from the efferent vessel, whether they are capillaries or smaller arterioles, has been termed the welling point. This area is visible on the surface of the kidney. The pattern of branching of the efferent vessel is suggestive of a “star” (Steinhausen, ’63). However, we found that only about 50% of the networks on the surface of the kidney have the “star” arrangement. The remaining patterns of the surface of the kidney do not have a star arrangement. The efferent vessel of these glomeruli rises to within 100 p m of the surface of the kidney and divides into two large branches each of which forms a peritubular network of capillaries. Therefore, for this efferent pattern the true welling point is not on the surface of the kidney and consequently is not accessible for micropuncture studies. From these studies, it is apparent that caution must be exer-
cised in sampling blood from the peritubular capillary system. Since there are several extensive studies of the vasa recta, our comments will be limited to the number of efferent vessels which arise from the juxtamedullary nephron. In the present study, a majority of these glomeruli have two branches, One branch remains in the cortical region, while the other descends to the medulla as the vasa recta. Conflicting reports in the literature on the pattern of efferent arterioles in the juxtamedullary area (Gksslen, ’34; Boenig, ’36; Ljungquist and Lagergren, ’62; Moffat and Fourman, ’63) may be due to filling defects which prevent all the branches of a n efferent arteriole from being visualized. ACKNOWLEDGMENTS
We would like to thank Pat Carlton and Judy DeLongo for their excellent technical help, and Paul Goodman for the art work. LITERATURE CITED Allison, M. E. M., E. Lipham and C. W. Gottschalk 1972 Hydrostatic pressure in the rat kidney. h e r . J. Physiol., 223: 975-983. Barger, A. C., and J. A. Herd 1973 Renal vascular anatomy and distribution of blood flow. In: Handbook of Physiology. Section 8. J. Orloff and R. W. Berliner, eds. American Physiological Society, Washington, D.C., pp. 249-313. Beeuwkes, R. 1971 Efferent vascular patterns and early vascular-tubular relations in the dog kidney. Amer. J. Physiol., 221; 1361-1374. Beeuwkes, R., and J. V . Bonventre 1975 Tubular organization and vascular-tubular relations in the dog kidney. h e r . J. Physiol., 229: 695714. Boenig, H. 1936 Beitrage zur Kenntnis der Vasa efferentiain dermenschlichen Niene. 2.mikranat. Forsch., 39: 105-115. Bowman, W. 1842 On the structure and use of the Malpighian bodies of the kidney with observations on the circulation through that gland. Phil. Trans. R. Soc. Ser., 1 : 57-80. Brenner, B. M., K. H. Falchuk, R. I. Keimowitz and R. W. Berliner 1969 The relationships between peritubular capillary protein concentration and fluid reabsorption by the proximal tubule. J. Clin. Invest., 48: 1519-1531. Brenner, B. M., and J. H. Galla 1971 Influence of post-glomerular hematocrit and protein concentration in rat nephron fluid transfer. Amer. J. Physiol., 220: 148-161. Brenner, B. M., and J. L. Troy 1971 Post-glomerular vascular protein concentrations. Evidence for a causal role in governing fluid reabsorption and glomerulotubular balance by the renal proximal tubule. J. Clin. Invest., 50: 336349.
EFFERENT VESSELS OF KIDNEY Burg, M. B., and J. Orloff 1968 Control of fluid absorption in the renal proximal tubule. J. Clin. Invest., 47: 2016-2024. Fourman, J., and D. B. Moffat 1971 The Blood Vessels of the Kidney. J . Fourman and D. B. Moffat, eds. Blackwell Scientific Publication, Oxford, pp. 90-114. Gansslen, M. 1934 Der feinere Gefassaufbau gesunder und Kranker menschlichen Nieren. Ergebn. inn. med. Kinderheilk, 47: 275420. Ljungquist, A., and C. Lagergren 1962 Normal intrarenal arterial pattern in adult and aging human kidney. J. Anat., 96: 285300. Martino, J. A., and L. E. Earley 1967 Demonstration of a role of physical factors as determinants of the natriuretic response to volume expansion. J. Clin. Invest., 46: 1953-1978. Moffat, D. B., and J . Fourman 1963 The vascular pattern of rat kidney. J. Anat., 97: 543-553.
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Mollendorff, W. von 1930 Der Erkretion-apparat i n Handblich der mikroscopischen Anatomie des Menschen 7, Berlin, Springer Verlag, pp. 107130. Seely, J. K. 1973 Effects of peritubular oncotic pressure on rat proximal tubule electrical resistance. Kid. Int., 4: 2 8 4 1 . Smith, J. P. 1956 Anatomical features of the human renal glomerular efferent vessel. J. Anat., 90: 290-292. Steinhausen, M . 1963 Eine Methode zur differenzierung proximalen und distalen tubuli der Nierenrinde von Ratten in vivo und ihre Anwendung zur Bestimmung tubularen Stromungsgeschwindigkeiten. Pfluger Arch. ges Physiol., 277: 2 3 4 5 . b e t a , J., A. E. Barclay, P.M. Daniel, K. J. Franklin and M. M. L. Prichard 1947 Studies of the Renal Circulation. Oxford, Blackwell.
PLATE I EXPLANATION OF FIGURES
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1
A low power view of the cortex of the rat kidney which has been injected with Microfil. This micrograph illustrates the three regions of the cortex which were studied: 0. outer, M, middle; I, inner. IL, interlobular artery. X 50.
2
A glomerulus in the outer cortex which has the l a type of efferent pattern (enlargement of an area i n fig. 1). Note the large diameter of the afferent arteriole (AA). The efferent arteriole (EA) is thin and branches at the capsule (arrows). X 200.
3
Efferent vessels of this glomerulus in the outer cortex have a type l b pattern. The efferent arteriole divides into two main branches well below the capsule. The welling point is indicated by the arrow. X 200.
4
Outer cortical glomerulus with the type l c efferent pattern. This pattern is characterized by an efferent vessel which divides into numerous branches beneath the capsule of the kidney. In this pattern there is not an identifiable welling point. X 200.
EFFERENT VESSELS OF KIDNEY Andrew P. Evan and William G. Dail, Jr
PLATE 1
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PLATE 2 EXPLANATION O F FIGURES
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5a-c
Branching patterns of efferent arterioles which lie directly beneath the capsule. The type l a pattern (fig. 2 ) resembles a “star” and has a distinct welling point (arrow). A more complex pattern arises from the two main branches of the type l b efferent arteriole (fig. 3). Figure 5b is a drawing of the “star” arrangement of the type l a efferent pattern and figure 5c illustrates the branching of type l b efferent pattern. 5a X 250; 5b X 250; 5c X 250.
6
In this example of a midcortical glomerulus, the efferent arteriole gives rise to a number of branches which form a complex capillary network lateral to the glomerulus. The branches do not rise to the capsule. x 200.
7
The efferent vessel of juxtamedullary glomeruli may divide immediately into a small cortical (arrow) and a larger medullary (double arrow) branch. The cortical branch forms a capillary bed in the vicinity of the glomerulus while the medullary branch descends into the medulla to form the vasa recta. X 150.
EFFERENT VESSELS OF KIDNEY Andrew P. Evan and William G. Dail, Jr.
PLATE 2
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PLATE 3 EXPLANATION
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O F FIGURES
Summary diagram of the branching pattern of efferent arterioles of the rat kidney. Three zones of the cortex (outer, middle and inner) may be defined by variations i n the branching pattern. In the outer cortex, the efferent arterioles branch at different levels to form three distinct types of glomerular efferents ( l a , lb, lc).
EFFERENT VESSELS OF KIDNEY Andrew P. Evan and William G. Dail, Jr
PLATE 3
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