The renal collecting system varies among domestic mammals. The renal pelvis as a common cavity around the renal crest in dogs, cats, sheep, and goats.1 In horses, the renal pelvis is a comparatively small central space with 2 terminal recesses extending into the renal poles.1 Renal calices are evident in cattle and pigs, but they are absent in other domestic mammals.1 In pigs2 and humans,3 a minor renal calyx surrounds the renal papilla and drains into the major renal calices, which join to form a renal pelvis. When compared with kidneys in other mammals, the kidneys of pigs and humans have differences in the morphology of the pelvicalyceal system, mainly in regard to the size and shape of the renal pelvis, with some renal pelvises lacking a dilatation.2,3
In 1 anatomy textbook,4 the renal calices are subordinated under the renal pelvis. A similar scheme for characteristic calyceal-type kidneys is reported in another anatomy textbook.5 However, the renal calyces are not subordinated under the renal pelvis in Nomina Anatomica Veterinaria,6 which leads to confusion, especially for the note referring to cattle that states that these animals do not have a renal pelvis but instead have renal calyces. However, it does not specify whether both major and minor renal calyces are present.6 Hence, the literature is laden with references to the presence of minor renal calyces1,7,8 or the presence of both minor and major renal calyces.9,10 The anatomy of the renal collecting system of cattle has generated controversial reports. In fact, there is general agreement that several minor renal calyces are present, but there are conflicting points of view regarding the existence of major renal calyces and a renal pelvis.1,7-9,11-14 Nomina Anatomica Veterinaria6 describes the renal pelvis as a dilatation at the end of the ureter and reports that the bovine kidneys have no such dilatation. Most textbooks of veterinary anatomy describe the bovine renal collecting system as lacking a renal pelvis at the end of the ureters.1,7-9,11-13 Furthermore, some authors depict the origin of the ureter as a simple junction of 2 ureteral branches1,7,8,12,13 or 2 major renal calyces,9 whereas other authors11,14 describe many major renal calyces and a tubular renal pelvis.
The kidneys of pigs are the most important renal tissues of domestic animals used for urological experiments because of their similarities with the kidneys of humans.2,15,16 Kidneys of other domestic animals, such as dogs17–22 and rabbits,23–26 have also been used in urological experiments. Kidneys of cattle have been used for the development of new techniques in laparoscopic partial nephrectomy.27,28 The use of bovine kidneys in urological research and the controversial nomenclature and description of the bovine renal collecting system in the literature have stimulated interest in the study of bovine renal anatomy. Recently, the external gross anatomy was evaluated and important differences, such as kidney length and size of the renal hilus, were identified between the kidneys of adult cattle and humans.29 However, there has not been a detailed description of the renal collecting system of cattle, which would aid understanding of the anatomy. Such a description would help researchers conduct reliable urological training. Therefore, the objective of the study reported here was to evaluate the collecting system of the kidneys of cattle and to propose a classification that would help resolve the controversy surrounding the anatomy of the bovine renal collecting system.
Materials and Methods
Sample population—Kidneys (n = 40) were collected from 20 adult male mixed-breed (Nelore X Angus) cattle (mean body weight, 480 kg; mean age, 3 years) immediately after slaughter at a slaughterhouse. All cattle underwent a clinical examination prior to slaughter, and inspections were performed during slaughter. The Institutional Animal Review Committee of the Serra dos Órgäos University Center approved the research protocol for the use of these bovine kidneys.
Procedures—A 3-D polyester resin corrosion endocast was made of the collecting system of each kidney. Casts were obtained by use of a technique described elsewhere.2 Briefly, a cannula was inserted into the ureter. Then, 15 to 20 mL of a yellow polyester resina was placed in a syringe. Methyl ethyl peroxideb (3% [by volume]) was added to the resin as a catalyst, and the materials were mixed. The resin mixture was manually injected via the cannula to fill the renal collecting system. All injections were performed by the same investigator (FSC). Resin was injected until the minor renal calyces could be palpated beneath the kidney surface and some resistance could be felt on the plunger of the syringe. Photographs were obtained of both surfaces of the kidney (dorsal and ventral) after the injection to record the identity of the cranial and caudal poles and the hilus region in the casts as well as the relationship between the renal lobes and the minor renal calices. The next day, the kidneys were immersed in a bath of concentrated hydrochloric acid (30%).c Kidneys were immersed for 48 hours to achieve total corrosion of the organic matter until only the cast of the renal collecting system remained.
Anatomic evaluation—For each kidney, the presence, shape, and size of the renal pelvis were determined at the origin of the ureter. The number of renal lobes and minor renal calyces in the entire kidney and in each renal region (cranial pole, caudal pole, and hilus) was recorded.
Statistical analysis—Differences in numbers for each variable were evaluated by use of an unpaired Student t test. Pearson correlations and Student t tests were used to estimate the linear correlation between the number of renal lobes and number of minor renal calyces. Length and thickness of the major renal calyces at the cranial and caudal poles were evaluated by use of an unpaired Student t test. Results were considered significant at values of P < 0.05.
Dorsal photographic views of resin casts of representative renal collecting systems of adult male cattle in which the renal pelvis has a lateral border (dotted line) that is convex (A) or concave (B). The medial aspect of the dilated funnel-shaped renal pelvis (p) is indicated (solid line; A and B), which is formed by the 2 major renal calyces (1 cranial [(cr] and 1 caudal [cd]) and continues into the ureter (u).
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Dorsal photographic views of resin casts of representative renal collecting systems of adult male cattle in which the renal pelvis has a lateral border (dotted line) that is convex (A) or concave (B). The medial aspect of the dilated funnel-shaped renal pelvis (p) is indicated (solid line; A and B), which is formed by the 2 major renal calyces (1 cranial [(cr] and 1 caudal [cd]) and continues into the ureter (u).
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Dorsal photographic views of resin casts of representative renal collecting systems of adult male cattle in which the renal pelvis has a lateral border (dotted line) that is convex (A) or concave (B). The medial aspect of the dilated funnel-shaped renal pelvis (p) is indicated (solid line; A and B), which is formed by the 2 major renal calyces (1 cranial [(cr] and 1 caudal [cd]) and continues into the ureter (u).
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Dorsal photographic views of resin casts of renal collecting systems of adult male cattle. A nondilated renal pelvis (p [circle]) is formed by the major renal calyces and continues into the ureter. A—The lateral border of the renal pelvis (arrow) is concave. B—The lateral border of the renal pelvis is marked by an incisure (arrowhead) between the 2 major renal calyces. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Dorsal photographic views of resin casts of renal collecting systems of adult male cattle. A nondilated renal pelvis (p [circle]) is formed by the major renal calyces and continues into the ureter. A—The lateral border of the renal pelvis (arrow) is concave. B—The lateral border of the renal pelvis is marked by an incisure (arrowhead) between the 2 major renal calyces. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Dorsal photographic views of resin casts of renal collecting systems of adult male cattle. A nondilated renal pelvis (p [circle]) is formed by the major renal calyces and continues into the ureter. A—The lateral border of the renal pelvis (arrow) is concave. B—The lateral border of the renal pelvis is marked by an incisure (arrowhead) between the 2 major renal calyces. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Results
Three casts were not in perfect condition. Therefore, the final analysis was conducted with the remaining 37 casts.
Schematic drawing of the 2 types of renal pelvis (dilated [A] and nondilated [B]) in bovine kidneys. See Figure 1 for key.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Schematic drawing of the 2 types of renal pelvis (dilated [A] and nondilated [B]) in bovine kidneys. See Figure 1 for key.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Schematic drawing of the 2 types of renal pelvis (dilated [A] and nondilated [B]) in bovine kidneys. See Figure 1 for key.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
The number of minor renal calyces per infundibulum in the major renal calyx of the cranial pole (A) and caudal pole (B) in the right kidney (white bars), left kidney (gray bars), and both kidneys (black bars) for 37 kidneys obtained from 20 adult male cattle. The percentages were calculated from the number of infundibula with the indicated number of minor renal calyces/the total number of infundibula per indicated region.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
The number of minor renal calyces per infundibulum in the major renal calyx of the cranial pole (A) and caudal pole (B) in the right kidney (white bars), left kidney (gray bars), and both kidneys (black bars) for 37 kidneys obtained from 20 adult male cattle. The percentages were calculated from the number of infundibula with the indicated number of minor renal calyces/the total number of infundibula per indicated region.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
The number of minor renal calyces per infundibulum in the major renal calyx of the cranial pole (A) and caudal pole (B) in the right kidney (white bars), left kidney (gray bars), and both kidneys (black bars) for 37 kidneys obtained from 20 adult male cattle. The percentages were calculated from the number of infundibula with the indicated number of minor renal calyces/the total number of infundibula per indicated region.
Citation: American Journal of Veterinary Research 71, 11; 10.2460/ajvr.71.11.1264
Length and thickness of the major renal calyces at the cranial and caudal pole of 37 kidneys obtained from 20 adult male cattle.
| Length | Thickness | |||
|---|---|---|---|---|
| Variable | Cranial | Caudal | Cranial | Caudal |
| Mean ± SD (mm) | 35.59 ± 9.22 | 34.93 ± 8.92 | 8.53 ± 1.76 | 9.39 ± 2.78 |
| CV (%) | 25.91 | 25.54 | 20.63 | 29.61 |
| Minimum (mm) | 11.87 | 17.24 | 4.55 | 5.58 |
| Maximum (mm) | 54.58 | 60.99 | 12.77 | 19.52 |
CV = Coefficient of variation.
The origin of the ureter was dilated in 9 of 37 (24.3%) casts of the renal collecting system (Figure 1). A dilated renal pelvis was less common (9/37 [24.3%] casts) than a nondilated renal pelvis and was represented by a large funnel-shaped cavity at the proximal end of the ureter. The lateral border of a dilated renal pelvis was either convex and bulging, caused by a branch arising from its lateral aspect, or was concave with a conical appearance.
In the remaining 28 (75.7%) casts, there was no dilatation and the origin of the ureter was formed by a funnel-like region at the union of the major renal calyces (Figure 2). A nondilated renal pelvis was more common (28/37 [75.7%] casts) and was represented by a small flared region in the proximal end of the ureter. The lateral border of a nondilated renal pelvis was concave or had an incisure at the junction of the 2 major renal calyces.
Therefore, a renal pelvis was present in all casts and could be classified into 2 types: nondilated and dilated (Figure 3).
All casts, with or without the dilated origin of the ureter, had a major renal calyx toward the cranial and the caudal poles. Length of the major renal calyx at the cranial and caudal poles ranged from 11.87 to 54.58 mm (mean, 35.59 mm) and from 17.24 to 60.99 mm (mean, 34.93 mm), respectively (Table 1).
The greatest thickness of the major renal calyx at the cranial and caudal poles ranged from 4.55 to 12.77 mm (mean, 8.53 mm) and from 5.58 to 19.52 mm (mean, 9.39 mm), respectively. Many minor renal calyces were connected to these 2 major renal calyces by an infundibulum; each infundibulum drained 1 to 6 minor renal calyces (Figure 4; Table 2).
The number of minor renal calyces per kidney ranged from 13 to 64 (mean, 22.7). The total number of minor renal calyces in each kidney and in each renal region (cranial pole, caudal pole, and hilus) was statistically analyzed (Table 3). Each bovine kidney had 13 to 25 renal lobes (mean, 20.6 renal lobes).
A significant correlation was detected between the number of renal lobes and the number of minor renal calyces for the entire kidney, the cranial pole region, and the hilus region (Table 4). However, there was not a significant correlation between the number of renal lobes and the number of minor renal calyces for the caudal pole region.
The number of renal lobes and the number of minor renal calyces differed significantly for the caudal pole region (Student t test, –4.41; P = 0.005) and the hilus region (Student t test, 4.47; P = 0.002). However, there was not a significant difference for the number of renal lobes and the number of minor renal calyces for the entire kidney (Student t test, —1.09; P = 0.353) and the cranial pole region (Student t test, –1.20; P = 0.312).
Discussion
In the study reported here, the renal pelvis was dilated in 9 of 37 (24.3%) casts. In the other 28 (75.7%) casts, there was no noticeable dilatation of the renal pelvis. Many authors1,7–10 describe the renal pelvis as the dilated proximal end of the ureter within the renal sinus; however, they report that the renal pelvis is absent in the kidneys of cattle. Those authors also indicate that the bovine ureter is formed by the junction of 2 ureteral branches1,7,8 or by the junction of the major renal calyces at the cranial and caudal poles,9,10 which differs from the results of the present study in which we identified a renal pelvis. Therefore, we propose that the renal pelvis was present in all casts and could be classified into 2 types (ie, nondilated and dilated; Figure 3). A nondilated renal pelvis was more common (28/37 [75.7%] casts) and represented a small flared region in the proximal end of the ureter. The lateral border of this type of renal pelvis was concave or had an incisure at the junction of the 2 major renal calyces (Figure 2). The lateral incisure made the lateral limit between the 2 major calyces more definitive. A dilated renal pelvis was less common (9/37 [24.3%] casts) and had a large funnel-shaped cavity at the proximal end of the ureter. The lateral border of this type of renal pelvis was convex, with a rounded appearance caused by a branch arising from it, or concave, with a conical morphological aspect (Figure 1).
Number of minor renal calices per infundibulum in the cranial pole region, caudal pole region, and the entire kidney for 37 kidneys obtained from 20 adult male cattle.
| Cranial pole | Caudal pole | ||||||
|---|---|---|---|---|---|---|---|
| No. of calyces/infundibulum | Right kidney | Left kidney | Total | Right kidney | Left kidney | Total | Entire kidney |
| 1 | 15.15 (10/66) | 37.04 (30/81) | 27.21 (40/147) | 21.79 (17/78) | 15.79 (12/76) | 18.83 (29/154) | 22.92 (69/301) |
| 2 | 46.97 (31/66) | 29.63 (24/81) | 37.41 (55/147) | 46.15 (36/78) | 44.74 (34/76) | 45.45 (70/154) | 41.53 (125/301) |
| 3 | 30.3 (20/66) | 17.28 (14/81) | 23.13 (34/147) | 21.79 (17/78) | 23.68 (18/76) | 22.73 (35/154) | 22.92 (69/301) |
| 4 | 3.03 (2/66) | 11.11 (9/81) | 7.48 (11/147) | 8.97 (7/78) | 9.21 (7/76) | 9.09 (14/154) | 8.31 (25/301) |
| 5 | 3.03 (2/66) | 2.47 (2/81) | 2.72 (4/147) | 1.28 (1/78) | 3.95 (3/76) | 2.6 (4/154) | 2.66 (8/301) |
| 6 | 1.52 (1/66) | 2.47 (2/81) | 2.04 (3/147) | 0 (0/78) | 2.63 (2/76) | 1.3 (2/154) | 1.66 (5/301) |
Values reported are percentages, which were calculated as the number of infundibula with the indicated number of calices/the total number of infundibula (shown in parentheses).
Number of minor renal calices and number of renal lobes in various regions of 37 kidneys obtained from 20 adult male cattle.
| Minor renal calyces | Renal lobes | |||||||
|---|---|---|---|---|---|---|---|---|
| Variable | Cranial pole | Hilus | Caudal pole | Total | Cranial pole | Hilus | Caudal pole | Total |
| Mean ± SD | 4.43 ± 2.47 | 7.19 ± 3.21 | 11.11 ± 7.16 | 22.73 ± 10.51 | 3.81 ± 2.01 | 11.05 ± 4.26 | 5.76 ± 2.14 | 20.62 ± 5.53 |
| CV (%) | 55.76 | 44.65 | 64.45 | 46.24 | 52.76 | 38.55 | 37.15 | 26.82 |
| Minimum | 1 | 3 | 2 | 13 | 1 | 5 | 2 | 13 |
| Maximum | 13 | 17 | 39 | 64 | 9 | 25 | 12 | 35 |
CV = Coefficient of variation.
Correlation between the number of renal lobes and the number of minor renal calices in various regions of 37 kidneys obtained from 20 adult male cattle.
| Renal region | Equation* | r | tvalve | Pvalue |
|---|---|---|---|---|
| Cranial pole | y = 1.05x ± 0.43 | 0.86 | 10.12 | 0.0002 |
| Hilus | y = 0.44x ± 2.38 | 0.58 | 4.28 | 0.0013 |
| Caudal pole | NA | 0.16 | 0.97 | 0.3856 |
| Entire kidney | y = 1.62x − 10.75 | 0.85 | 9.63 | 0.0004 |
For each equation, y is the number of minor renal calices and x is the number of renal lobes.
NA = Not applicable.
In Nomina Anatomica Veterinaria,6 the renal calyces are not subordinated to the renal pelvis because there is no description of a renal pelvis in cattle, at least as a dilatation at the end of the ureter. In domestic mammals and humans, the renal collecting system (ie, the renal pelvis and its subdivisions [including the renal calyces]) forms embryologically as an outgrowth of the ureteric bud. In calyceal-type kidneys, the major renal calyces subdivide into many minor renal calyces to drain the renal papilla.5 However, there is controversy as to the presence of major renal calyces in cattle because of the numerous interpretations by different authors. This adds to the controversy concerning the presence of a renal pelvis in the bovine renal collecting system. Detailed evaluation of the renal collecting systems of pigs2 and humans3 revealed differences in the types of the renal pelvis.3 In a classification of the renal collecting system in humans, investigators reported3 various types of renal pelvis, including a small renal pelvis similar to that found in cattle in the present study. Similar to humans, the renal collecting system of pigs was evaluated and classified as a small renal pelvis2 by the use of endocasts. Because porcine and human kidneys may have a small renal pelvis, a small renal pelvis would not be unexpected in bovine kidneys.
All casts, with or without the dilated origin of the ureter, had 2 branches (1 toward the cranial pole and 1 toward the caudal pole). These branches are considered by some authors1,7,8 as the cranial and caudal branches of the ureter; however, to resolve the controversy, it would be more correct to consider these as major renal calyces because they drain the minor renal calyces to the renal pelvis via several branches of various sizes (Figures 1 and 2). Because the renal pelvis is evident at the origin of the ureter, it would be better to consider the tubular extensions of the renal pelvis as major renal calyces instead of as ureteral branches because they are not connected to the ureters but instead are connected to the renal pelvis. By assigning this nomenclature to the bovine renal collecting system, confusion could be eliminated and terms could be standardized and harmonized with those of the human and porcine kidneys because the ureteric bud is developmentally responsible for this tubular system in mammals.5 In contrast, other authors11–14 report that the renal pelvis is located at the proximal end of the ureter, without dilatation, and is formed by 2 long cylindrical tubes that directly receive the minor renal calyces12,13 or that receive many major renal calyces draining the minor renal calyces.11,14 In the study reported here, minor renal calyces were connected via an infundibulum to the major renal calyces of the cranial and caudal poles. These connections have been termed major calyces by some authors,11,14 whereas other authors12,13 do not mention these structures and instead report that the minor renal calyces drain directly into the long ureteral branches.
Mean length of the major renal calyces associated with the cranial and caudal poles was 35.59 and 34.93 mm, respectively. The greatest mean thickness of the major renal calyces at the cranial and caudal poles was 8.53 and 9.39 mm, respectively. Minor renal calyces were connected to the 2 major calyces by an infundibulum, which drained 1 to 6 minor renal calyces. The most frequent situation was 1 infundibulum draining 2 minor renal calyces (125/301 [41.5%] infundibula), except in the cranial pole of the left kidneys, where the most common situation was 1 infundibulum draining 1 minor renal calyx (30/81 [37.0%] infundibula). In addition, the correlation between the number of renal lobes and the number of minor renal calyces has not been studied before. The number of renal lobes varied significantly among the renal areas, with the greatest number of renal lobes in the hilus region (mean, 11.1 renal lobes) and the smallest number of renal lobes in the cranial pole region (mean, 3.8 renal lobes; Table 3). We detected significant correlations between the number of renal lobes and the number of renal minor calyces in the cranial pole region, the hilus region, and the entire kidney. However, we did not detect a significant correlation between the number of renal lobes and the number of renal minor calyces in the caudal pole region.
The hilus region had significantly (P = 0.002) more renal lobes (11.1) than minor renal calyces (7.2). This finding is in agreement with results of other reports12,13; in those studies, investigators found 4 and 2 to 3 papillae/minor renal calyx, respectively. In contrast, the caudal pole had significantly (P = 0.005) more minor renal calyces (11.1) than renal lobes (5.8). This suggested that in the caudal pole, the cortex of the renal lobes could be fused externally, which would correspond to ≥ 1 pyramid internally.
In this study, each bovine kidney had from 13 to 64 minor renal calyces (mean, 22.7 minor renal calyces). This range differs substantially from values reported in other studies (15 to 20 minor renal calyces12 and 18 to 24 minor renal calyces1,11,14). No other investigators have detected such a large number (> 30) of minor renal calyces. Furthermore, the mean number of minor renal calyces varied significantly (P ≤ 0.01) among the renal regions, with the greatest number of minor renal calyces in the caudal pole region and the smallest number of minor renal calyces in the cranial pole region. The number of minor renal calyces in the kidneys of cattle is greater than that in the kidneys of pigs2 (range, 4 to 19; mean, 8.2) or humans3 (range, 5 to 14; mean, 8.2).
In the present study, major and minor renal calyces in the kidneys of cattle were extremely narrow, compared with those in pigs2 and humans.3 Therefore, bovine kidneys are not appropriate for use as a model in endourologic training, especially for researchers for which intrarenal access is of utmost importance (eg, in situations when researchers need to use a nephroscope).2
The bovine renal collecting system is variable and has 2 types of renal pelvis (dilated and nondilated). The renal pelvis has 2 major renal calyces (1 cranial and 1 caudal) that are connected to several minor renal calyces by an infundibulum. This characterization of the bovine renal collecting system is suitable for comparison with that of other domestic mammals and is an attempt to resolve the controversy regarding the presence of a renal pelvis and major renal calyces.
Resina polyester cristal, Resi-line Comercial ltda, Rio de Janeiro, Brazil.
Catalisador MEK, Resi-line Comercial ltda, Rio de Janeiro, Brazil.
Ácido muriático, Dipil Indústria Química, Massaranduba, Brazil.
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