The Renal Vascular System of the Monkey: a Gross Anatomical Description MARK J
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J. Anat. (1987), 153, pp. 123-137 123 With 8 figures Printed in Great Britain The renal vascular system of the monkey: a gross anatomical description MARK J. HORACEK, ALVIN M. EARLE AND JOSEPH P. GILMORE Departments ofAnatomy and Physiology and Biophysics, University of Nebraska College of Medicine, Omaha, Nebraska 68105, U.S.A. (Accepted 12 September 1986) INTRODUCTION Monkeys are frequently used as a model for physiological experiments involving the kidney. It is known that physiological disparity between mammalian species can often be elucidated by a study of the structural differences between these species. Despite this fact, the monkey's renal vasculature has not been described in sufficient detail. Such a description would be useful since monkey experimentation plays an important role in understanding human physiology. Also, the branching pattern and segmen- tation of the monkey's renal vasculature is interesting from both comparative and experimental viewpoints. Fourman & Moffat (1971) indicated that although all mammalian kidneys are somewhat similar, there are several species-specific differences in terms oforganisation, microstructure and function. They conducted several extensive vascular studies on mammals, including several rodents and carnivores, but did not include any specific information concerning the monkey. Graves (1971) and Fine & Keen (1966) have described the branching patterns and segmentation of human kidneys. However, comparable information pertaining to the monkey kidney is not available. The purpose of the present study is to provide a detailed morphological description of the gross renal vasculature in the kidneys of two species of monkeys, Macacafascicularis and Macaca mulatta. MATERIALS AND METHODS Twelve monkeys (Macacafascicularis and Macaca mulatta) were used in this study after they had been utilised for electrophysiological experimentation. Before death by pentobarbital sodium overdose, all monkeys were heparinised with 2 ml of sodium heparin (10000 units/ml) and their vascular systems were dilated by injection with papavarine hydrochloride. Perfusion techniques Following death, the thoracic aorta was mobilised and a polyethylene cannula was inserted and tied in position. The inferior vena cava was incised just above the diaphragm to allow the blood to escape during perfusion. Following this, 1000 ml of isotonic saline containing 10 units/ml of sodium heparin were perfused through the aortic cannula. Each monkey was then perfused with either neoprene latex 842A (Nebraska Scientific, Omaha, NE) or Batson's no. 17 anatomical corrosion compound (Polysciences, Inc., Warrington, PA). In some cases both compounds were used, one being perfused into the arterial and the other into the venous system. 5-2 124 M. J. HORACEK, A. M. EARLE AND J. P. GILMORE Perfusion of the arterial system with Batson's compound The arterial system of five monkeys was perfused with Batson's no. 17 anatomical corrosion compound coloured with Batson's red or blue pigment. After completing the heparinised saline perfusion, a cannula, connected to a 25 ml syringe, was inserted into the thoracic aorta and secured with a ligature. Following a five minute interval, 20 ml of compound was injected into the aorta using moderate, constant pressure, never forcing the injection when resistance was noted. (A five minute delay was allowed to increase the viscosity of the perfusion compound and thereby avoid perfusion of the smaller vessels.) Following perfusion, pressure in the system was maintained while the thoracic aorta was ligated just distal to the cannula. The injected compound was allowed to harden in a refrigerator overnight. Gross anatomical observations of the renal artery and its associated structures were made prior to subsequent dissection to isolate the trunk region. After the dissection, the remaining tissue, which included the diaphragm, pelvis and intervening tissue with its blood supply, was placed in a container and cleared in a solution of 5 % sodium hydroxide. The resulting vascular cast was stored in 5 % formalin. Perfusion of the arterial system with neoprene latex 842A Following the initial saline perfusion, the arterial system of three monkeys was perfused with neoprene latex 842A. The arterial system of each monkey was studied in situ, and then corroded and stored in 5 % sodium hydroxide solution using methods similar to those described above. Perfusion of the venous system In addition to the eight monkeys utilised for arterial perfusions, the venous system of two monkeys was perfused through the inferior vena cava. Following the initial saline perfusion, a cannula connected to a 25 ml syringe was inserted into the inferior vena cava just above the diaphragm and secured with a ligature below the diaphragm just superior to the renal veins. One monkey was perfused with neoprene latex 842A and the other with Batson's no. 17 anatomical corrosion compound. After refrigeration to allow time for cast hardening the kidneys and adjacent tissues were placed in a 5 % sodium hydroxide solution for corrosion. After corrosion, the Batson's cast was stored in 10 % formalin while the latex cast was stored in a 5 % sodium hydroxide solution. Combined arterial and venous perfusions Following the initial saline perfusion, in two monkeys Batson's compound was perfused into the arterial system prior to the perfusion of neoprene latex 842A into the venous system. These perfusions and subsequent corrosion and storage in 5 % formalin were accomplished using methods similar to those described above. RESULTS The renal artery The course of the renal artery in the monkey (Macaca fascicularis and Macaca mulatta) and its relationship to other structures is similar to that observed in man. The renal arteries arise from the lateral aspect of the aorta below the superior mesenteric artery at approximately the same level, although either may arise more cranially than its counterpart on the contralateral side. Similarly, the kidneys sometimes lie at Renal vascular system ofmacaque monkey 125 approximately the same level, or one or the other may lie cranial to its partner. A kidney lying above its contralateral partner is sometimes, in fact, supplied by a renal artery with an origin below its contralateral partner. Consequently, the path of each renal artery is variable, taking a horizontal, superolateral, or inferolateral course (Fig. 1). At, or slightly before reaching the hilum of the kidney, the renal artery divides into an anterior and a posterior division. Each division branches into segmental arteries, the most proximal portions of which can often be seen at the hilum and traced into the sinus of the kidney. At the hilum, the renal vein lies anterior to the renal artery and/or its divisions, and the renal pelvis is posterior and inferior to both the renal vein and artery. However, because the posterior division of the renal artery eventually passes posterior to the renal pelvis, the proximal portions of the posterior segmental arteries regularly lie posterior to the pelvis. Each renal artery may give rise to one or more inferior suprarenal arteries along its course. More distally, and frequently near the hilum, small vessels are -given off to the renal capsule and to the proximal portion of the ureter. Occasionally, capsular vessels arise from the anterior and posterior divisions of the renal artery. Capsular vessels also often arise from one or more of the inferior suprarenal arteries. In a few cases the inferior phrenic artery was a branch ofthe proximal portion ofthe renal artery (Fig. 1). Arterial segmentation of the kidney Each division of the renal artery branches into arteries each of which supplies a distinct area or segment of renal parenchyma. The size of these arterial segments, and each segment's particular vascular supply, was somewhat variable from one kidney to another, even when comparing kidneys from the same monkey. Despite the variability encountered, all sixteen kidneys could be categorised into the general segmentation scheme described below. The anterior division of the renal artery supplies approximately the anterior half of the kidney, while the posterior division supplies the posterior half, although either division may supply slightly more or less than half of the kidney. When the perfusion of casting compound is such that the glomeruli do not fill, it is possible to observe this anterior and posterior arterial division along the convex border of the kidney. In man, this division has been called Br6del's line and in the monkey is always variable in its longitudinal course so that no straight line can define, with any specificity, the parenchymal regions supplied by the anterior or posterior divisions of the renal artery. When the perfusion of casting compound results in the filling of glomeruli and efferent arterioles, this division or line between anterior and posterior arterial regions of the kidney is not discernible. This is because glomeruli of adjacent segments lie in close proximity to one another (although there are no apparent anastomoses between them) and this tight juxtaposition obscures the longitudinal line of demarcation described above. Anterior segments The anterior region of the kidney may be divided into three or four segments of variable size, each segment generally receiving its blood supply from one segmental artery. Occasionally more than one artery may supply a renal segment. This may occur when the normal segmental artery is replaced by two smaller arteries having a similar origin, or when an adjacent segmental artery distributes what might be interpreted as an anomalous branch to a segment other than its own. From superior to inferior, the four anterior segments of the kidney are the apical, 126 M. J. HORACEK, A. M. EARLE AND J. P. GILMORE 3. IA I p- . w a. IF ,, t 1%. I X.V:.6s 7-.I..I .I it I N I */ ..q ... .. A .C Renal vascular system ofmacaque monkey 127 upper, middle and lower segments. Figures 2 and 3 are schematic representations of the approximate area of supply of each anterior segmental artery. Notice that occasionally the apical segment is replaced by an enlarged area of supply by the upper segment.