PERIRENAL FASCIA

The perirenal fascia is a dense, elastic connective tissue sheath which envelops each kidney and suprarenal gland together with a layer of surrounding perirenal fat (Fig. 74.4A,B; see Fig. 62.1). The kidney and its vessels are embedded in perirenal fat, which is thickest at the renal borders and extends into the renal sinus at the hilum.

Fig. 74.4 A, Sagittal section through the posterior abdominal wall showing the relations of the renal fascia of the right kidney. B, Transverse section, showing the relations of the renal fascia.

The perirenal fascia was originally described as being made up of two separate entities, the posterior fascia of Zuckerkandl and the anterior fascia of Gerota, which fused laterally to form the lateral conal fascia. According to this view, the lateral conal fascia continued anterolaterally behind the colon to blend with the parietal peritoneum. However, work by Mitchell (1950) showed that the perirenal fascia is not made up of distinct fused fasciae, but is in fact a single multilaminated structure which is fused posteromedially with the muscular fasciae of psoas major and quadratus lumborum. It then extends anterolaterally behind the kidney as a bilaminated sheet, which at a variable point divides into a thin anterior lamina, passing around the front of the kidney as the anterior perirenal fascia, and a thicker posterior lamina which continues anterolaterally as the lateral conal fascia, fusing with the parietal peritoneum.

Classically, the anterior perirenal fascia was thought to blend into the dense mass of connective tissue surrounding the great vessels in the root of the mesentery behind the duodenum and pancreas, thereby preventing communication between perirenal spaces across the midline. However inspection of CT images or of anatomical sections of cadavers, following injection of contrast or coloured latex respectively, into the perirenal space, revealed that fluid could extend across the midline at the third to fifth lumbar levels through a narrow channel measuring 2–10 mm in AP dimension. In the midline superiorly, the anterior and posterior renal fasciae fuse and are attached to the crura of their respective hemidiaphragms. Inferiorly the fasciae separate for a variable craniocaudal distance. The posterior perirenal fascia fuses with the muscular fascia of psoas major while the anterior perirenal fascia extends across the midline in front of the great vessels and so communication between the two sides is permitted although very rarely of clinical significance. Below this level the two fasciae once again merge and are attached to the great vessels or iliac vessels. The containment of fluid to one side of the perirenal space that is observed in over two thirds of clinical cases is attributed to the presence of fibrous septae.

Above the suprarenal glands the anterior and posterior perirenal fasciae were previously said to fuse with each other and to the diaphragmatic fascia. This description of a closed superior cone is not universally accepted. Cadaveric experiments have shown the superior aspect of the perirenal space to be open and in continuity with the bare area of the liver on the right and the subphrenic extraperitoneal space on the left. The posterior fascial layer blends bilaterally with the fascia of psoas major and quadratus lumborum as well as the inferior phrenic fascia. The anterior fascial layer on the right blends with the right inferior coronary ligament at the level of the upper pole of the kidney and bare area of the liver. On the left the anterior layer fuses with the gastrosplenic ligament at the level of the suprarenal gland.

There is some debate concerning the inferior fusion of the perirenal fascia. Many investigators believe that inferiorly the anterior and posterior leaves of the perirenal fascial fuse to produce an inverted cone which is open to the pelvis at its apex. Laterally the anterior and posterior leaves fuse with the iliac fascia, and medially they fuse with the periureteric connective tissue. The inferior apex of the cone is open anatomically towards the iliac fossa but rapidly becomes sealed in inflammatory disease. An alternative view is based on the dissection of recently deceased cadavers after injections of coloured latex into the perirenal space: these have shown that the anterior and posterior perirenal fasciae merge to form a single multilaminar fascia which contains the ureter in the iliac fossa. Anteriorly this common fascia is loosely connected to the parietal peritoneum, and so denies free communication between the perirenal space and the pelvis, and also denies communication between the perirenal and pararenal spaces.

A simple nephrectomy for benign disease removes the kidney from within perirenal fascia; a radical nephrectomy (for cancer) removes the entire contents of the perirenal space including the perirenal fascia, in order to give adequate clearance around the tumour.

RELATIONS

The superior poles of both kidneys are thick and round and each is related to its suprarenal gland (Fig. 74.5A,B). The inferior poles are thinner and extend to within 2.5 cm of the iliac crests. The lateral borders are convex. The medial borders are convex adjacent to the poles, concave between them and slope inferolaterally. In each a deep vertical fissure opens anteromedially as the hilum, which is bounded by anterior and posterior lips and contains the renal vessels and nerves and the renal pelvis. The relative positions of the main hilar structures are the renal vein (anterior), the renal artery (intermediate) and the pelvis of the kidney (posterior). Usually an arterial branch from the main renal artery runs over the superior margin of the renal pelvis to enter the hilum on the posterior aspect of the pelvis, and a renal venous tributary often leaves the hilum in the same plane. Above the hilum the medial border is related to the suprarenal gland and below to the origin of the ureter.

Fig. 74.5 Ventral aspect of left kidney and suprarenal gland (A), and of right kidney and suprarenal gland (B). Note the left suprarenal vein enters the left renal vein. This is an important relationship to identify when performing a left nephrectomy.

(From Sobotta 2006.)

The convex anterior surface of the kidney actually faces anterolaterally and its relations differ on the right and left. Likewise the posterior surface of the kidneys in reality faces posteromedially. Its relations are similar on both sides of the body (Fig. 74.6A–D).

Fig. 74.6 Multislice CT scan of the kidneys. A, Axial CT scan of the kidneys showing the anatomical relationships of the kidneys at the renal hilum. B, Coronal reformat showing both kidneys and the suprarenal glands. C, Sagittal reformat of the left kidney lying posterior to the stomach, spleen and pancreas. D, Sagittal reformat of the right kidney lying posterior to the right lobe of the liver, hepatic flexure and duodenum.

A small area of the superior pole is in contact with the right suprarenal gland, which may overlap the upper part of the medial border of the superior pole. A large area below this is immediately related the right lobe of the liver separated by a layer of peritoneum. A narrow medial area is directly related to the retroperitoneal descending part of the duodenum. Inferiorly the anterior surface is directly in contact laterally with the retroperitoneal right colic flexure and medially with part of the intraperitoneal small intestine.

A small medial area of the superior pole is related to the left suprarenal gland. The lateral half of the anterior surface is related to the spleen from which it is separated by a layer of peritoneum. A central quadrilateral area lies in direct contact with the retroperitoneal pancreas and the splenic vessels. Above this a small variable triangular region, between the suprarenal and splenic areas, is in contact with the stomach separated by a layer of peritoneum. Below the pancreatic and splenic areas, a narrow lateral strip which extends to the lateral border of the kidney is directly related to the retroperitoneal left colic flexure and the beginning of the descending colon. An extensive medial area is related to intraperitoneal loops of jejunum. The gastric area is covered with the peritoneum of the lesser sac (omental bursa) and the splenic and jejunal areas are covered by the peritoneum of the greater sac. Behind the peritoneum covering the jejunal area, branches of the left colic vessels are related to the kidney (Fig. 74.7A,B).

Fig. 74.7 Surfaces of the kidneys. A, Anterior, showing the areas related to neighbouring viscera. The areas where overlying viscera are separated from the kidney by peritoneum are shown. B, Posterior, showing the areas of relation to the posterior abdominal wall.

(From Drake, Vogl, Mitchell, Tibbitts and Richardson 2008.)

The posteromedial surface of the kidneys is embedded in fat and devoid of peritoneum. The right and left kidneys are related to similar structures. Superiorly are the diaphragm and the medial and lateral arcuate ligaments. More inferiorly, moving in a medial to lateral direction, are psoas major, quadratus lumborum and the aponeurotic tendon of transversus abdominis, the subcostal vessels and the subcostal, iliohypogastric, and ilioinguinal nerves. The upper pole of the right kidney is level with the 12th rib, and that of the left with the 11th and 12th ribs. The diaphragm separates the kidney from the pleura, which descends to form the costodiaphragmatic recess: diaphragmatic muscle is sometimes defective or absent in a triangle immediately above the lateral arcuate ligament, and this allows perirenal adipose tissue to contact the diaphragmatic pleura.

INTERNAL MACROSTRUCTURE

The postnatal kidney has a thin fibrous capsule composed of collagen-rich tissue with some elastic and smooth muscle fibres. In renal disease the capsule may become adherent (Fig. 74.8A,B).

Fig. 74.8 Left kidney, oblique vertical hemisection: normal macroscopic appearance of the renal cortex and renal medulla and the major structures at the hilum of the kidney. In A, the fat body of the renal sinus and most of the major vessels at the hilum have been removed, and the renal pelvis has not been opened. In B, the renal pelvis has been opened to reveal the interlobar arteries.

(B from Sobotta 2006.)

The kidney itself can be divided into an internal medulla and external cortex. The renal medulla consists of pale, striated, conical renal pyramids, their bases peripheral, their apices converging to the renal sinus. At the renal sinus they project into calyces as papillae.

The renal cortex is subcapsular, arching over the bases of the pyramids and extending between them towards the renal sinus as renal columns. Its peripheral regions are termed cortical arches and are traversed by radial, lighter-coloured medullary rays, separated by darker tissue, the convoluted part. The rays taper towards the renal capsule and are peripheral prolongations from the bases of renal pyramids. The cortex is histologically divisible into outer and inner zones. The inner zone is demarcated from the medulla by tangential blood vessels (arcuate arteries and veins), which lie at the junction of the two, however a thin layer of cortical tissue (subcortex) appears on the medullary side of this zone. The cortex close to the medulla is sometimes termed the juxtamedullar cortex.

Renal pelvis and calyces

The hilum of the kidney leads into a central renal sinus, lined by the renal capsule and almost filled by the renal pelvis and vessels, the remaining space being filled by fat. Dissection into this plane can be challenging but is important in surgery on the renal pelvis, particularly open stone surgery. Within the renal sinus, the collecting tubules of the nephrons of the kidney open onto the summits of the renal papillae to drain into minor calyces, which are funnel-shaped expansions of the upper urinary tract. The renal capsule covers the external surface of the kidney and continues through the hilum to line the sinus and fuse with the adventitial coverings of the minor calyces. Each minor calyx surrounds either a single papilla or, more rarely, groups of two or three papillae. The minor calyces unite with their neighbours to form two or possibly three larger chambers, the major calyces. There is wide variation in the arrangement of the calyces. As the posterior aspect of the kidney rotates laterally during its ascent in utero, the calyces which were lateral in utero become positioned anteriorly, and the medial calyces move more posteriorly. The calyces drain into the infundibula. The renal pelvis is normally formed from the junction of two infundibula, one from the upper and one from the lower pole calyces, but there may be a third, which drains the calyces in the mid-portion of the kidney. The calyces are usually grouped so that three pairs drain into the upper pole infundibulum and four pairs into the lower pole infundibulum. If there is a middle infundibulum, the distribution is normally three pairs at the upper pole, two in the middle, and two at the lower pole. There is considerable variation in the arrangement of the infundibula and in the extent to which the pelvis is intrarenal or extrarenal. The funnel-shaped renal pelvis tapers as it passes inferomedially, traversing the renal hilum to become continuous with the ureter (Fig. 74.8A,B; see Fig. 74.9). It is rarely possible to determine precisely where the renal pelvis ceases and the ureter begins: the region is usually extrahilar and normally lies adjacent to the lower part of the medial border of the kidney. Rarely, the entire renal pelvis has been found to lie inside the sinus of the kidney so that the pelviureteric region occurs either in the vicinity of the renal hilum or completely within the renal sinus.

Fig. 74.9 A, Conventional intravenous urogram showing the renal calyces, pelves and both ureters. 1. Ureter. 2. Bladder. 3. Renal pelvis. 4. Calyces. B, Multislice CT urogram. 3D-surface shaded reformat showing the kidneys, ureters, bladder and surrounding bony anatomy.

The calyces, renal pelvis and ureter are well-demonstrated radiologically following an intravenous injection of radio-opaque contrast which is excreted in the urine (intravenous urography – IVU) (Fig. 74.9A,B); or after the introduction of radio-opaque contrast into the ureter by catheterization through a cystoscope (ascending or retrograde pyelography. Normal cupping of the minor calyces by projecting renal papillae may be obliterated by conditions that cause hydronephrosis, chronic distension of the ureter and renal pelvis due to upper or lower urinary tract obstruction resulting in elevated intrapelvic pressure. An appreciation of the rotation of the kidneys which results in the posterior calyces lying relatively medially and the anterior calyces lying laterally is essential when interpreting contrast imaging of the collecting system of the kidneys.

VASCULAR SUPPLY AND LYMPHATIC DRAINAGE

Renal arteries

The paired renal arteries take about 20% of the cardiac output to supply organs that represent less than one-hundredth of total body weight. They branch laterally from the aorta just below the origin of the superior mesenteric artery (see Fig. 62.8; Fig. 74.10A). Both cross the corresponding crus of the diaphragm at right angles to the aorta. The right renal artery is longer and often higher, passing posterior to the inferior vena cava, right renal vein, head of the pancreas, and descending part of the duodenum. The left renal artery is a little lower and passes behind the left renal vein, the body of the pancreas, and splenic vein. It may be crossed anteriorly by the inferior mesenteric vein.

Fig. 74.10 A, Axial multislice CT renal angiogram. B, Variations in the number and patterns of branching of the renal artery (percentages are approximate).

(B from Sobotta 2006.)

A single renal artery to each kidney is present in approximately 70% of individuals (Fig. 74.11). The arteries vary in their level of origin and in their calibre, obliquity and precise relations (Fig. 74.10B). In its extrarenal course each renal artery gives off one or more inferior suprarenal arteries, a branch to the ureter and branches which supply perinephric tissue, the renal capsule, and the pelvis. Near the renal hilum, each artery divides into an anterior and a posterior division, and these divide into segmental arteries supplying the renal vascular segments. Accessory renal arteries are common (30% of individuals), and usually arise from the aorta above or below (most commonly below) the main renal artery and follow it to the renal hilum. They are regarded as persistent embryonic lateral splanchnic arteries. Accessory vessels to the inferior pole cross anterior to the ureter and may, by obstructing the ureter, cause hydronephrosis. Rarely, accessory renal arteries arise from the coeliac or superior mesenteric arteries near the aortic bifurcation or from the common iliac arteries.

Fig. 74.11 Resin corrosion cast of human kidneys. Ureters, pelves and calyces are yellow; aorta, renal arteries and their branches are red.

(Prepared by the late DH Tompsett of the Royal College of Surgeons of England. By permission of the Museums of The Royal College of Surgeons.)

The subdivisions of the renal arteries are described sequentially as segmental, lobar, interlobar, arcuate and interlobular arteries and afferent and efferent glomerular arterioles (see Fig. 74.14).

Fig. 74.14 The major structures in the kidney cortex and medulla (left), the position of cortical and juxtamedullary nephrons (middle) and the major blood vessels (right).

Segmental arteries

Renal vascular segmentation was originally recognized by John Hunter in 1794, but the first detailed account of the primary pattern was produced in the 1950s from casts and radiographs of injected kidneys. Five arterial segments have been identified (Fig. 74.12). The apical segment occupies the anteromedial region of the superior pole. The superior (anterior) segment includes the rest of the superior pole and the central anterosuperior region. The inferior segment encompasses the whole lower pole. The middle (anterior) segment lies between the anterior and inferior segments. The posterior segment includes the whole posterior region between the apical and inferior segments. This is the pattern most commonly seen, and although there can be considerable variation it is the pattern that clinicians most frequently encounter when performing partial nephrectomy. Whatever pattern is present, it must be emphasized that vascular segments are supplied by virtual end arteries. In contrast, larger intrarenal veins have no segmental organization and anastomose freely.

Fig. 74.12 Segmental arterial anatomy of the right kidney: the posterior division branches near the hilum before the anterior division divides into the other segmental arteries.

Brödel (1911) described a relatively avascular longitudinal zone (the ‘bloodless’ line of Brödel) along the convex renal border, which was proposed as the most suitable site for surgical incision. However, many vessels cross this zone, and it is far from ‘bloodless’: planned radial or intersegmental incisions are preferable. Knowledge of the vascular anatomy of the kidney is important when undertaking partial nephrectomy for renal cell cancers. In this surgery the branches of the renal artery are defined so that the surgeon may safely excise the renal substance containing the tumour while not compromising the vascular supply to the remaining renal tissue.

Lobar, interlobar, arcuate and interlobular arteries

The initial branches of segmental arteries are lobar, usually one to each renal pyramid. Before reaching the pyramid they subdivide into two or three interlobar arteries, extending towards the cortex around each pyramid. At the junction of the cortex and medulla, interlobar arteries dichotomize into arcuate arteries which diverge at right angles. As they arch between cortex and medulla, each divides further, ultimately supplying interlobular arteries which diverge radially into the cortex. The terminations of adjacent arcuate arteries do not anastomose but end in the cortex as additional interlobular arteries. Though most interlobular arteries come from arcuate branches, some arise directly from arcuate or even terminal interlobar arteries (see Fig. 74.14). Interlobular arteries ascend towards the superficial cortex or may branch occasionally en route. Some are more tortuous and recurve towards the medulla at least once before proceeding towards the renal surface. Others traverse the surface as perforating arteries to anastomose with the capsular plexus (which is also supplied from the inferior suprarenal, renal and gonadal arteries).

Afferent and efferent glomerular arterioles

Afferent glomerular arterioles are mainly the lateral rami of interlobular arteries. A few arise from arcuate and interlobar arteries when they vary their direction and angle of origin: deeper ones incline obliquely back towards the medulla, the intermediate pass horizontally, and the more superficial approach the renal surface obliquely before ending in a glomerulus (see Fig. 74.14). Efferent glomerular arterioles from most glomeruli (except at juxtamedullary and, sometimes, at intermediate cortical levels) soon divide to form a dense peritubular capillary plexus around the proximal and distal convoluted tubules: there are thus two sets of capillaries, glomerular and peritubular, in series in the main renal cortical circulation, linked by efferent glomerular arterioles. The vascular supply of the renal medulla is largely from efferent arterioles of juxtamedullary glomeruli, supplemented by some from more superficial glomeruli, and ‘aglomerular’ arterioles (probably from degenerated glomeruli). Efferent glomerular arterioles passing into the medulla are relatively long, wide vessels, and contribute side branches to neighbouring capillary plexuses before entering the medulla, where each divides into 12–25 descending vasa recta. As their name suggests, these run straight to varying depths in the renal medulla, contributing side branches to a radially elongated capillary plexus (see Fig. 74.14) applied to the descending and ascending limbs of renal loops and to collecting ducts. The venous ends of capillaries converge to the ascending vasa recta, which drain into arcuate or interlobular veins. An essential feature of the vasa recta (particularly in the outer medulla) is that both ascending and descending vessels are grouped into vascular bundles, within which the external aspects of both types are closely apposed, bringing them close to the limbs of renal loops and collecting ducts. As these bundles converge centrally into the renal medulla they contain fewer vessels: some terminate at successive levels in neighbouring capillary plexuses. This proximity of descending and ascending vessels with each other and adjacent ducts provides the structural basis for the countercurrent exchange and multiplier phenomena (see countercurrent exchange mechanism later in chapter (see Fig. 74.17)). These complex renal vascular patterns show regional specializations which are closely adapted to the spatial organization and functions of renal corpuscles, tubules and ducts (see below).

Fig. 74.17 The regional microstructure and principal activities of a kidney nephron and collecting duct. For clarity, a nephron of the long loop (juxtamedullary) type is shown.

Renal veins

Fine radicles from the venous ends of the peritubular plexuses converge to join interlobular veins, one with each interlobular artery. Many interlobular veins begin beneath the fibrous renal capsule by the convergence of several stellate veins, which drain the most superficial zone of the renal cortex and so are named from their surface appearance. Interlobular veins pass to the corticomedullary junction and also receive some ascending vasa recta before ending in arcuate veins (which accompany arcuate arteries), and anastomose with neighbouring veins. Arcuate veins drain into interlobar veins, which anastomose and form the renal vein.

The large renal veins lie anterior to the renal arteries and open into the inferior vena cava almost at right angles. The left is three times longer than the right (7.5 cm and 2.5 cm respectively) and for this reason, the left kidney is the preferred side for live donor nephrectomy. The left renal vein runs from its origin in the renal hilum, posterior to the splenic vein and the body of pancreas, and then across the anterior aspect of the aorta, just below the origin of the superior mesenteric artery. The left gonadal vein enters it from below and the left suprarenal vein, usually receiving one of the left inferior phrenic veins, enters it above but nearer the midline. The left renal vein enters the inferior vena cava a little superior and to the right. The right renal vein is behind the descending duodenum and sometimes the lateral part of the head of the pancreas. It can be extremely short (<1 cm) such that safe nephrectomy may require excision of a cuff of the inferior vena cava (Fig. 74.13).

Fig. 74.13 CT renal venogram. Acquired from a multislice CT examination and reconstructed as a 3D surface shaded reformat.

The left renal vein may be double, one vein passing posterior, the other anterior, to the aorta before joining the inferior vena cava. This is sometimes referred to as persistence of the ‘renal collar’. The anterior vein may be absent so that there is a single retroaortic left renal vein. The left renal vein may be ligated during surgery for aortic aneurysm because it has such a close relationship with the aorta: this seldom results in any harm to the kidney, provided that the ligature is placed to the right of the draining gonadal and suprarenal veins, since these usually provide adequate collateral venous drainage. The right renal vein has no significant collateral drainage and cannot be ligated with impunity.

INNERVATION

Rami from the coeliac ganglion and plexus, aorticorenal ganglion, lowest thoracic splanchnic nerve, first lumbar splanchnic nerve and aortic plexus form a dense plexus of autonomic nerves around the renal artery.

Small ganglia occur in the renal plexus, the largest usually behind the origin of the renal artery. The plexus continues into the kidney around the arterial branches and supplies the vessels and renal glomeruli, and especially the cortical tubules. Axons from plexuses around the arcuate arteries innervate juxtamedullary efferent arterioles and vasa recta, which control the blood flow between the cortex and medulla without affecting the glomerular circulation. Axons from the renal plexus contribute to the ureteric and gonadal plexuses.

MICROSTRUCTURE

The kidney is composed of many tortuous, closely packed uriniferous tubules, bounded by a delicate connective tissue in which run blood vessels, lymphatics and nerves. Each tubule consists of two embryologically distinct parts, the nephron, which produces urine, and the collecting duct, which completes the concentration of urine and through which urine passes out into the calyces of the kidney, the renal pelvis, the ureter and urinary bladder (see p. 1305).

Nephron

The nephron consists of a renal corpuscle, concerned with filtration from the plasma, and a renal tubule, concerned with selective resorption from the filtrate to form the urine (Fig. 74.14). Collecting ducts carry fluid from several renal tubules to a terminal papillary duct, opening into a minor calyx at the apex of a renal papilla. Papillary surfaces show numerous minute orifices of these ducts and pressure on a fresh kidney expresses urine from them.

Renal corpuscle

Renal corpuscles are small rounded structures averaging 0.2 mm in diameter, visible in the renal cortex deep to a narrow peripheral cortical zone (Fig. 74.15A,B). Each has a central glomerulus of vessels and a glomerular (Bowman’s) capsule, from which the renal tubule originates.

Fig. 74.15 A, Low power view of the kidney showing renal cortex (Ct) comprising glomeruli (G), proximal and distal convoluted tubules (T) and blood vessels (BV). The medulla (M) contains loops of Henle and collecting ducts (CD) (× 20, H&E stain). B, A glomerulus with a network of capillaries (C) set within a small amount of connective tissue, the mesangium (M). The glomerular basement membrane (GBM) of the capillaries is continuous with the Bowman’s capsule (BC) of the glomerulus, and is separated from it by Bowman’s space (BS) (× 200, H&E stain).

There are about one million renal corpuscles in each kidney, their number (which may be determined in part by intra-uterine factors) decreases with age; this process is accelerated by raised blood pressure. After birth new nephrons cannot be developed – a lost nephron can never be replaced. The decrease in corpuscular numbers with age is reflected in a corresponding reduction in the rate of glomerular filtration from the fourth decade onwards.

Glomerulus

A glomerulus is a collection of convoluted capillary blood vessels, united by a delicate mesangial matrix and supplied by an afferent arteriole which enters the capsule opposite the urinary pole, where the filtrate enters the tubule. (The term glomerulus is used most frequently to describe the entire renal corpuscle.) An efferent arteriole emerges from the same point, the vascular pole of the corpuscle. Glomeruli are simple in form until late prenatal life; some remain so for about 6 months after birth, the majority maturing by 6 years and all by 12 years (see p. 1305).

Bowman’s capsule

Bowman’s capsule is the blind expanded end of a renal tubule, and is deeply invaginated by the glomerulus. It is lined by a simple squamous epithelium on its outer (parietal) wall; its glomerular, juxtacapillary (visceral) wall is composed of specialized epithelial podocytes. Between the two walls of the capsule is a flattened urinary (Bowman’s) space, continuous with the proximal convoluted tubule (Fig. 74.15B; see Fig. 74.17).

Podocytes are stellate cells. Their major (primary) foot processes curve around the capillary loops and branch to form secondary processes which are applied closely to the basal lamina; secondary or tertiary processes give rise to terminal pedicels (Fig. 74.16A). Pedicels of one cell alternate with those of an adjacent cell and interdigitate tightly with each other, separated by narrow (25 nm) gaps, the filtration slits (Fig. 74.16B). The latter are covered by a dense, membranous slit diaphragm, through which filtrate must pass to enter the urinary space. The differentiation of the adult podocyte phenotype is associated with the presence of several specific proteins, including nephrin, podocin, synaptopodin and GLEPP-1. Mutations in these proteins can cause important functional problems, e.g. the classical Finnish form of congenital nephritic syndrome is caused by a mutation of NHPS1 coding for nephrin. The luminal membrane and the slit diaphragm are covered by a dense surface coat rich in sialoglycoproteins, which gives this surface a very high negative charge and is one of the key characteristics of the perm-selectivity barrier. Differentiated podocytes cannot replicate.

Fig. 74.16 A, Podocytes forming the visceral layer of Bowman’s capsule in the renal corpuscle. Their cell bodies (P) send out primary processes which branch several times and end in fine pedicels which wrap tightly around the glomerular capillaries (C), and interdigitate with similar pedicels from a neighbouring podocyte. B, The glomerular filtration apparatus is formed by the endothelial cells of fenestrated capillaries, the filtration slits between podocyte pedicels and their thick shared basal lamina. BL, basal lamina; C, capillary loops; E, endothelial cell cytoplasm; F, fenestrations; FS, filtration slits; P, podocyte, P₁ and P₂, primary and secondary foot processes which rest on the glomerular basal laminae.

(By permission of Igaku-Shoin, Tokyo, from Fujita T, Tanaka K, Tokunaga J 1981 SEM Atlas of Cells and Tissues). (By permission from Young B, Heath JW 2000 Wheater’s Functional Histology. Edinburgh: Churchill Livingstone.)

The glomerular endothelium is finely fenestrated. The principal barrier to the passage of fluid from capillary lumen to urinary space is the glomerular basal lamina, the fused endothelial and podocyte basal laminae. This is usually 0.33 μm thick in man, and acts as a selective filter, allowing the passage from blood, under pressure, of water and various small molecules and ions in the circulation. Haemoglobin may cross the filter, but larger molecules and those of similar size with a negative charge, are largely retained. Most protein that does enter the filtrate is selectively resorbed and degraded by cells of the proximal convoluted tubule.

The glomerular basement membrane (GBM) serves as the skeleton of the glomerular tuft. Its outer aspect is completely covered by podocytes, and the interior is filled by capillaries and a delicate mesangial matrix (mesangium). The major components of the GBM are laminin and type IV collagen (both of which are expressed as unique isoforms) and heparin sulphate proteoglycans.

Irregular mesangial cells, with phagocytic and contractile properties, lie within and secrete the glomerular mesangium, a specialized connective tissue which binds the loop of glomerular capillaries and fills the spaces between endothelial surfaces that are not invested by podocytes (Fig. 74.15B; see Fig. 74.17). Mesangial cells are related to vascular pericytes and are concerned with the turnover of glomerular basement membrane. They clear the glomerular filter of immune complexes and cellular debris, and their contractile properties help to regulate blood flow. Similar cells, the extraglomerular mesangial (lacis) cells, lie outside the glomerulus at the vascular pole and form part of the juxtaglomerular apparatus.

Renal tubule

A renal or uriniferous tubule consists of a glomerular capsule that leads into a proximal convoluted tubule connected to the capsule by a short neck and continuing into a sinuous or coiled convoluted part (Fig. 74.17). This straightens as it approaches the medulla, and becomes the descending thick limb of the loop of Henle and then the ascending limb by an abrupt U-turn. The limbs of the loop of Henle are narrower and thin-walled within the deeper medullary tissue where they become the descending and ascending thin segments. The ascending thick limb continues into the distal tubule. The tubule wall shows a focal thickening, the macula densa, where it comes close to the vascular pole of its parent glomerulus at the start of the convoluted part of the distal tubule. The nephron finally straightens once more as the connecting tubule, which ends by joining a collecting duct.

Collecting ducts originate in the cortical medullary rays and join others at intervals. They finally open into wider papillary ducts which open on to a papilla, their numerous orifices forming a perforated area cribrosa on the surface at its tip (Fig. 74.14).

Renal tubules are lined throughout by a single-layered epithelium (Figs 74.17, 74.18). The type of epithelial cell varies according to the functional roles of the different regions, e.g. active transport and passive diffusion of various ions and water into and out of the tubules; reabsorption of organic components such as glucose and amino acids; uptake of any proteins which leak through the glomerular filter.

Fig. 74.18 Part of the renal medulla in cross-section. Note large collecting ducts and small thin segments of the loop of Henle, interspersed with vasa recta (V) (trichrome stained).

The proximal convoluted tubule is lined by cuboidal or low columnar epithelium and has a brush border of tall microvilli on its luminal surface. The shape of the cells depends on tubular fluid pressure, which in life distends the lumen and flattens the cells (they become taller when glomerular blood pressure falls postmortem or at biopsy). The cytoplasm of proximal tubular cells is strongly eosinophilic and the nuclei are euchromatic and central. The basal cytoplasm is rich in mitochondria, orientated perpendicularly, and the basal plasma membrane is highly infolded. The lateral surfaces of adjacent epithelial cells interdigitate, increasing the complexity of the basolateral plasma membrane. The microvilli on the luminal surfaces significantly increase the area of plasma membrane in contact with tubular fluid and the extratubular space, facilitating the transport of ions and small molecules against steep concentration gradients. The abundant mitochondria supply the energy, as ATP, needed for this process. Sodium/potassium adenosine triphosphatase (Na/K ATPase) is located in apical and basal membranes, and the cytoplasm contains numerous other enzymes concerned with ion transport. Water and other solutes pass between cells (paracellular transport) passively along osmotic and electrochemical gradients, probably through leaky apical tight junctions. Pinocytotic vesicles are found near the apical surface, and represent the means by which small proteins and peptides from the filtrate are internalized and degraded by associated lysosomes. Peroxisomes and lipid droplets abound in the cytoplasm.

The loop of Henle consists of a thin segment (30 μm in diameter), lined by low cuboidal to squamous cells, and a thick segment (60 μm in diameter) composed of cuboidal cells like those in the distal convoluted tubule. The thin segment forms most of the loop in juxtamedullary nephrons which reach deep into the medulla. Few organelles appear in cells lining the thin segment, indicating that these cells play a passive, rather than an active, role in ion transport. The thick segment is composed of cuboidal epithelium with many mitochondria, deep basolateral folds and short apical microvilli, indicating a more active metabolic role. The thick limb of the loop of Henle is the source of Tamm–Horsfall protein in normal urine.

Cells of the distal tubule are cuboidal and resemble those in the proximal tubule. They have few microvilli, and so the tubular lumen has a more distinct outline. The basolateral folds containing mitochondria are deep, almost reaching the luminal aspect (Fig. 74.17). Enzymes concerned in active transport of sodium, potassium and other ions are abundant. At the junction of the straight and convoluted regions the distal tubule comes close to the vascular pole of its parent renal corpuscle. Here, tubular cells form the macula densa, a sensory structure which is concerned with the regulation of blood flow and thus filtration rate. Cells in the terminal part of the distal tubule have fewer basal folds and mitochondria and constitute a connecting duct formed from metanephric mesenchyme during embryogenesis. Collecting ducts are lined by simple cuboidal or columnar epithelium. This increases in height from the cortex, where the ducts receive the contents of distal tubules, to the wide papillary ducts which discharge at the area cribrosa. The pale-staining principal cells have relatively few organelles or lateral interdigitations and only occasional microvilli. A second cell type, intercalated or dark cells (also present in smaller numbers in the distal convoluted tubule), have longer microvilli and more mitochondria and secrete H⁺ into the filtrate; they function in the maintenance of acid–base homeostasis.

PRODUCTION OF URINE

RELATIONS

In the abdomen the ureter descends posterior to the peritoneum on the medial part of psoas major, which separates it from the tips of the lumbar transverse processes. During surgery on intraperitoneal structures, the ureter can be tented up as the peritoneum is drawn anteriorly, resulting in inadvertent ureteric injury. Anterior to psoas major it crosses in front of the genitofemoral nerve and is obliquely crossed by the gonadal vessels (Fig. 74.19). It enters the lesser pelvis anterior to either the end of the common iliac vessels or at the origin of the external iliac vessels (Fig. 74.20).

Fig. 74.19 Relations of lower ureter. A, Male pelvis. B, Female pelvis.

(From Drake, Vogl and Mitchell 2005.)

Fig. 74.20 Relations of male lower right ureter.

(By permission from Walsh PC, Retik AB, Vaughan ED et al (eds) 2002 Campbell’s Urology, 8th edn. Philadelphia: Saunders.)

The inferior vena cava is medial to the right ureter while the left ureter is lateral to the aorta. The inferior mesenteric vein has a long retroperitoneal course lying close to the medial aspect of the left ureter.

At its origin the right ureter is usually overlapped by the descending part of the duodenum. It descends lateral to the inferior vena cava, and is crossed anteriorly by the right colic and ileocolic vessels. Near the superior aperture of the lesser pelvis it passes behind the lower part of the mesentery and terminal ileum. The left ureter is crossed by the gonadal and left colic vessels (see Fig. 74.24). It passes posterior to loops of jejunum and sigmoid colon and its mesentery in the posterior wall of the intersigmoid recess.

Fig. 74.24 Arterial supply of the left ureter. The proximal part takes its blood supply medially, and the distal part is supplied laterally.

(By permission from Walsh PC, Retik AB, Vaughan ED et al (eds) 2002 Campbell’s Urology, 8th edn. Philadelphia: Saunders.)

In the pelvis the ureter lies in extraperitoneal areolar tissue (see Fig. 75.3). At first it descends posterolaterally on the lateral wall of the lesser pelvis along the anterior border of the greater sciatic notch. Opposite the ischial spine it turns anteromedially into fibrous adipose tissue above levator ani to reach the base of the bladder. On the pelvic side-wall it is anterior to the internal iliac artery and the beginning of its anterior trunk, posterior to which are the internal iliac vein, lumbosacral nerve and sacroiliac joint. Laterally it lies on the fascia of obturator internus. It progressively crosses to become medial to the umbilical, inferior vesical, and middle rectal arteries.

In males, the pelvic ureter hooks under the vas deferens (Fig. 74.21), then passes in front of and slightly above the upper pole of the seminal vesicle to traverse the bladder wall obliquely before opening at the ipsilateral trigonal angle. Its terminal part is surrounded by tributaries of the vesical veins. In females, the pelvic part at first has the same relations as in males, but anterior to the internal iliac artery it is immediately behind the ovary, forming the posterior boundary of the ovarian fossa (see Ch. 77). In the anteromedial part of its course to the bladder it is related to the uterine artery, uterine cervix and vaginal fornices. It is in extraperitoneal connective tissue in the inferomedial part of the broad ligament of the uterus where it may be damaged during hysterectomy. In the broad ligament, the uterine artery is anterosuperior to the ureter for 2.5 cm and then crosses to its medial side to ascend alongside the uterus. The ureter turns forwards slightly above the lateral vaginal fornix and is generally 2 cm lateral to the supravaginal part of the uterine cervix in this location. It then inclines medially to reach the bladder, with a variable relation to the anterior aspect of the vagina. As the uterus is commonly deviated to one side, one ureter, usually the left, may be more extensively apposed to the vagina, and may cross the midline.

Fig. 74.21 Posterior aspect of the male urogenital organs, showing relationship of the lower ureter to the vas deferens and seminal vesicles.

(From Sobotta 2006.)

The distal 1–2 cm of each ureter is surrounded by an incomplete collar of non-striated muscle, which forms a sheath (of Waldeyer). The ureters pierce the posterior aspect of the bladder and run obliquely through its wall for a distance of 1.5–2.0 cm before terminating at the ureteric orifices (see Fig. 75.5B). This arrangement is believed to assist in the prevention of reflux of urine into the ureter, since the intramural ureters are thought to be occluded during increases in bladder pressure at the time of micturition. There is no evidence of a classic ureteral sphincter mechanism in man. The longitudinally oriented muscle bundles of the terminal ureter continue into the bladder wall and at the ureteric orifices become continuous with the superficial trigonal muscle. In the distended bladder, in both sexes, the ureteric openings are usually 5 cm apart, and 2.5 cm apart when the bladder is empty.

Duplex ureters

In 1 in 125 individuals, two ureters drain the renal pelvis on one side; this is termed a duplex system (Fig. 74.22). Bilateral duplex ureters occur in approximately 1 in 800 cases. The duplex ureters derive from two ureteric buds arising from the mesonephric duct. They are contained in a single fascial sheath and may fuse at any point along their course or may be separate until they insert through separate ureteric orifices into the bladder. Care must be taken not to compromise the blood supply of the second ureter when excising or reimplanting a single ureter of a duplex.

Fig. 74.22 Intravenous urogram showing bilateral duplex ureters and bilateral ureteroceles. Note that the ureters cross during their course. The right ureterocele can be clearly seen producing a halo appearance within the bladder surrounding the lower ureter. 1. Contrast within lower moiety of collecting system. 2. ‘Cobra’s head’ halo around lower ureter showing ureterocele. 3. Contrast within upper moiety of collecting system.

The ureter from the upper pole of the kidney (the longer ureter) inserts more medially and caudally in the bladder than the ureter from the lower pole (the shorter ureter). This reflects the embryological development of the ureter: the ureteric bud which is initially more proximal on the mesonephric duct has a shorter time to be pulled cranially in the bladder and so it inserts more distally in the mature bladder. The ureter from the lower pole has a shorter intramural course than the longer ureter and is prone to reflux.

Ectopic ureters

Single ureters, and more commonly the longer ureter of a duplex system, can insert more caudally and medially than normal in some individuals. In the male the ureter can insert at the bladder neck or posterior urethra, or rarely into the seminal vesicle, but it always inserts cranial to the external urethral sphincter. In the female, ectopic insertion can be distal to the external urethral sphincter in the urethra, or into the vagina, resulting in persistent childhood incontinence.

Ureteroceles

A ureterocele is a cystic dilatation of the lower end of the ureter: the ureteric orifice is covered by a membrane which expands as it is filled with urine and then deflates as it empties. Ureteroceles can vary in size, and although usually they have no influence on ureteric drainage they can be a cause of obstruction in the ureter and pelvicalyceal system more proximally. They usually do not cause bladder outflow obstruction except for the rare prolapsing ureterocele. Prolapsing ureteroceles, though small, prolapse from their position around the uretero-vesical junction region in to the urethra, causing intermittent bladder outflow obstruction. They are identified antenatally with ultrasound. In adults, ureteroceles tend to be bilateral and small and often found incidentally when the urinary tract is being imaged in the investigation of a coincidental pathology. Radiologically they classically result in a ‘cobra-head’ halo around the ureteric orifice following administration of contrast on intravenous urography (Fig. 74.22).

Retrocaval ureter

A persistence of the posterior cardinal vein, associated with high confluence of the right and left common iliac veins or a double inferior vena cava, may result in a retrocaval (or circumcaval) ureter which passes behind the inferior vena cava, usually at the level of the inferior edge of the third part of the duodenum, before it emerges in front of it to pass from medial to lateral. Retrocaval ureter occurs in 1 in 1500 individuals. Most commonly it has no clinical sequelae although it can result in upper ureteric obstruction (Fig. 74.23).

Fig. 74.23 Intravenous urogram showing a classical retrocaval (or circumcaval) ureter. A degree of obstruction has resulted in a markedly dilated upper ureter. The ureter passes cranially, medially and then caudally, and can be followed into the pelvis. 1. Contrast within dilated collecting system of right kidney and upper ureter. 2. Contrast within ureter turning behind inferior vena cava. 3. Contrast within normal calibre ureter seen below the obstruction. 4. Contrast within normal collecting system of left kidney and upper ureter.

VASCULAR SUPPLY AND LYMPHATIC DRAINAGE

INNERVATION

The ureter is supplied from the lower three thoracic, first lumbar, and the second to fourth sacral segments of the spinal cord by branches from the renal and aortic plexuses, and the superior and inferior hypogastric plexuses. The ureteric nerves consist of relatively large bundles of axons which form an irregular plexus in the adventitia of the ureter. The plexus receives branches from the renal and aortic plexuses (in its upper part), from the superior hypogastric plexus and hypogastric nerve (in its intermediate part), and from the hypogastric nerve and inferior hypogastric plexus (in its lower part). Numerous small branches penetrate the ureteric muscle coat: some of the adventitial nerves accompany the blood vessels and branch with them as they extend into the muscle layer, others are unrelated to the vascular supply and lie free in the adventitial connective tissue around the circumference of the ureter.

The density of innervation increases gradually from the renal pelvis and upper ureter (where autonomic nerves are sparse) to a maximum density in the juxtavesical segment. At least three different neurotransmitter phenotypes, cholinergic, noradrenergic and peptidergic (substance P), are well known and others have been reported. The functional significance of these different types of autonomic nerve fibres in relation to ureteric smooth muscle activity is not fully understood: although they are thought to influence the inherent motility of the ureter, they are not essential for the initiation and propagation of ureteric contraction waves. A branching plexus of fine cholinergic, noradrenergic and peptidergic axons occurs throughout the lamina propria and extends from the inner aspect of the muscle coat towards the base of the urothelium. Some of these axons form perivascular plexuses, others lie in isolation from the vascular supply and may be sensory in function.

RENAL AND URETERIC CALCULI

An understanding of intrarenal and ureteric anatomy is essential when managing patients with calculi, particularly now that minimally invasive techniques are widely used to treat this common pathology.

Smaller renal calculi are treated with extracorporeal shock wave lithotripsy. Stones in the lower pole of the kidney clear less well if the angle between the infundibulum of the calyx containing the stone and the ureter is acute, or if there is a particularly long and narrow infundibulum. Percutaneous stone extraction is most frequently achieved by puncturing a posterior calyx with a needle.

Ureteric calculi tend to be arrested in their descent in either the pelviureteric region, or the point where the ureter passes over the pelvic brim as it crosses the common iliac artery, or the vesico-ureteric junction, because these are the three areas where the ureter is narrowest. The vesico-ureteric junction is the narrowest of these areas and can be responsible for arresting the passage of stones of as little as 2–3 mm.

The kidney and upper ureter move with respiration within the perirenal fascia, and this can affect the visualization and tracking of a stone, both at the time of extracorporeal shock wave lithotripsy and at retrograde endoscopy.

MICROSTRUCTURE

Like the calyces and the renal pelvis, the wall of the ureter is composed of an external adventitia, a smooth muscle layer and an inner mucosal layer (Fig. 74.25). The mucosal layer consists of a urothelium and an underlying connective tissue lamina propria.

Fig. 74.25 Transverse section of ureter. The walls are muscular and are lined by a specialized urothelium.

(By permission from Stevens A, Lowe JS 1996 Human Histology, 2nd edn. London: Mosby.)

The ureteric adventitial blood vessels and connective tissue fibres are orientated parallel to the long axis of the ureter. Throughout its length, the muscle coat of the ureter is fairly uniform in thickness and in cross-section measures 750–800 μm in width. The muscle bundles which constitute this coat are frequently separated from one another by relatively large amounts of connective tissue. However, branches which interconnect muscle bundles are common and there is frequent interchange of muscle fibres between adjacent bundles. As a consequence of this extensive branching, individual muscle bundles do not spiral around the ureter, but form a complex meshwork of interweaving bundles. Moreover, unlike the gut (see Ch. 66), the muscle bundles are so arranged that morphologically distinct longitudinal and circular layers cannot be clearly distinguished. In the upper part of the ureter, the inner muscle bundles tend to lie longitudinally while those on the outer aspect have a circular or oblique orientation. In the middle and lower parts, there are additional outer longitudinally orientated fibres, and as the ureterovesical junction is approached, the muscle coat consists predominantly of longitudinally orientated muscle bundles.

The mucosa of the ureter consists of an epithelium, the urothelium, on the deep aspect of which is a layer of subepithelial fibroelastic connective tissue lamina propria. The latter varies in thickness from 350–700 μm and is a conduit for small blood vessels and bundles of non-myelinated nerve fibres. Occasional lymphocytes may be present in the lamina propria but their aggregation into definitive lymph nodules is rare. The urothelium is usually extensively folded, which gives the ureteric lumen a stellate outline.