The Intrarenal Venous Architecture of the Pig Kid- Ney (Sus Scrofa)

Venous Architecture of pig kidney Farag,F.M.M.

The Intrarenal Venous Architecture of the Pig Kid- ney (Sus scrofa)

Farag, F.M.M.

Anatomy Department, Faculty of Veterinary Medicine, Cairo University, EGYPT

With 9 figures. Received August, accepted for publication December 2012

Abstract throughout the renal parenchyma and on that basis we conclude that The aim of the present study was to the renal venous system in the pig explore the intrarenal ramifications is not segmented. Our results are of the renal vein in the kidney of the compared to those in other animal pig. For this purpose, the kidneys of species and in humans. eight adult pigs of both sexes were used. Corrosion casting and Keywords: Pig Kidney, intra-renal, radiography revealed that the main venous architecture. stem renal vein was formed by the union of three renal veins, cranial, Introduction middle and caudal. The 3nd order of Many animals have been used as branching was represented by 8-9 experimental models for urologic interlobar veins. The ventral half of procedures. The pig kidney is often the cranial end and the caudal third used due to the resemblance of its of the kidney were drained by the structural features to those of the cranial and caudal renal veins as human kidney (Sampaio et al., 1998 well as their large interlobar and Pereira-Sampaio et al., 2004). tributaries. The dorsal half was The pig kidney is also frequently drained by small dorsal collateral used in the nephrolithotomy as a veins that emptied into the ventral model for research (Kaouk et al., set. In the middle third of the organ, 2003) and training (Hammond et al., there were large veins in a close 2004 and Erap, 2003). Urologists relationship to the ventral and have been looking for a better dorsal surface of the uretero-pelvic method to control bleeding during junction in 75% and 25% of the and after endourological procedures specimens respectively. Numerous (Jua et al, 2004). Many studies venous anastomoses were found

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Venous Architecture of pig kidney Farag,F.M.M. have been done on the anatomy of Two approaches to injection were the pig kidney, including its employed: one to visualize the veins morphometric aspects (Sampaio et in 3-dimensions in a plastic cast; al,1998) , the collecting system and and one for a radiological view arterial relationships (Pereira- using a radio-opaque filler material Sampaio et al, 2004) as well as the without corrosion. intrarenal venous arrangement (Vo- denicharov and gulubova, 1995 and 1- Cast formation: This was com- Filho et al, 2008). However, this posed of blue Kem-epoxy No. 151/ study is undertaken to extend know- 20, a mixture of solutions A/B in a ledge of the intrarenal tributaries of ratio of 3:1 respectively. The speci- the renal vein, as a way to help mens were kept at room tempera- urologists in experimental research ture for 4 days then corroded in and urological surgical training 10% KOH for 4-6 weeks, then when using the pig as an animal rinsed with a gentle stream of water. model. 2- Radio – opaque visualization: Material and Methods This was composed of a 30% suspension of red lead oxide color- The kidneys of eight adult pigs of less in Kem-epoxy No. 150. 2A:1B. both sexes were used for this study. It was examined at 55 k v 30-70 In addition, five pig feti were used to MA, 0.5 second and FFd 70 cm. demonstrate the origin of the renal The specimens were photographed veins. Eight fresh unfixed kidneys using Olympus digital camera SP- (four rights and four left) were used 600UZ 12 mega pixel. for cast formation, these were manually dissected before corrosion The results obtained were dis- to demonstrate the relationship cussed and compared with those of between the intrarenal veins and other authors who performed earlier the collecting system. The remai- studies in the pig and other animals. ning eight kidneys were used for the radiographic study. The specimens The nomenclature used here is that were injected through the stem of the Nomina Anatomica Veteri- renal vein and in two specimens naria (2005). Some additional terms only the cranial and caudal renal were used based on that in the veins were injected separately extant literatures which may not be visualize the anastomoses between recorded in the N.A.V. these veins.

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Results portion of the renal hilus. However in six of the examined specimens V. renalis the cranial renal vein was formed The principal renal vein (Figs 1-9/1) only by three interlobar veins (I,II was represented by a single vessel and III), while the fourth (IV) one per each kidney entering the caudal emptied into the middle renal vein. vena cava on a level between the Moreover, the cranial renal vein re- 2nd and 3rd lumbar vertebra. The ceived three dorsal collateral veins right renal vein joined the vena cava A and B and C that drained the cor- slightly more cranial than the left responding dorsal portion. The one in three of the dissected pig veins A (Figs 3 , 4/14) drained the embryos while in other two both most cranial polar portion through veins joined the vena cava at the 2-3 tributaries and emptied into the same level. The left renal vein dorsal aspect of the interlobar vein I crossed the ventral surface of the (12 specimens) or II (4 specimens). abdominal aorta and was relatively The vein B (Figs 3 , 4/15) drained longer than the right one. The main the caudal portion of the cranial 3rd stem renal vein was fed by three by 3-4 tributaries and terminated renal veins, cranial, middle and into the dorsal aspect of the cranial caudal. Each of these veins was renal vein ( 10 specimens) or the responsible for the venous drainage interlobar vein IV (6 specimens). of a corresponding portion of the The vein C (Figs 3, 4/16) drained kidney via a variable number of in- the dorsal aspect of the ureteropel- terlobar veins in the ventral half of vic region through two radicals and the kidney, ventral to the collecting opened into the cranial renal vein system while the dorsal half of the near its origin. kidney was drained through smaller dorsal collateral veins that emptied V. renalis medius into the dorsal aspects of these The middle renal vein (Figs 1-9/3) trunks. was the smallest of the three main venous trunks of the stem renal V. renalis cranialis vein. It measured about 2.0 cm in The cranial renal vein (Figs 1-9/2) length and was formed by the union arose in the cranial portion of the of two middle interlobar veins (V kidney by the confluence of four and VI) which drained the middle cranial interlobar veins (I-IV), pro- third of the ventral half of the kidney ceeded caudally for about 2-3 cm (hilar zone). It also received one before it emerged from the cranial dorsal collateral vein D (Figs 3 , 4/

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17) that drained the corresponding collateral branches (E) and (F) that dorsal portion of the renal paren- drained the corresponding dorsal chyma through two main tributaries. half of the renal parenchyma. The The middle renal vein proceeded vein E (Fig. 3 and 4/18) was the ventral to the collecting system in largest of the dorsal collateral veins. 12 specimens and dorsal to it in the It drained the cranial portion of the other 4 specimens. In only two of caudal 3rd just caudal to the hilar the examined specimens the middle zone of the kidney by 4-5 tributaries renal vein joined the stem renal vein that radiated caudally towards the while in 12 specimens it emptied caudal pole of the kidney. The vein into either the cranial renal vein F (Fig. 3 and 4/19) drained the most (Figs 1-4 and 8) or into the caudal caudal portion (caudal polar region) renal vein (Figs 5-7) in an equal through 2-3 small radicles and percent. In the remaining two spec- emptied into the dorsal aspect of imens the stem middle renal vein the interlobar vein IX (13 speci- was absent (Fig 9) and the interlo- mens) or VIII (3 specimens). How- bar veins V and VI drained into the ever in four other specimens the cranial and caudal renal veins re- later vein was absent and the spectively. tributaries of the vein E extended to the caudal pole of the kidney. V. renalis caudalis The caudal renal vein (Figs 1-9/4) Vv. Interlobares from point of its size and direction The interlobar veins where repre- represented the direct continuation sented by 8-9 vessels that formed of the stem renal vein. It was near the corticomedullary junction formed in the caudal portion of the by the confluence of the arcuate kidney by the confluence of three veins and extended ventral to the caudal interlobar veins which could main collecting ducts then between be designated as interlobar veins the calyces minor and medullary VII, VIII and IX that drained the pyramids and joined forming the caudal third of the ventral half of the three main renal veins. These can kidney. It swerved cranially for be numbered in Roman numerals about 2.5 cm caudal to the ureter from I-IX and differentiated into then emerged from the caudal three groups; cranial, middle and portion of the renal hilus and caudal. Those from I to IV ( Figs 2- emptied into the stem renal vein. It 5/ 5,6,7,8) represented the cranial is necessary to add that the caudal group that formed the cranial renal renal vein also received two dorsal vein and drain the corresponding

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Venous Architecture of pig kidney Farag,F.M.M. third of the ventral half of the organ, were formed by the confluence of while the interlobar veins V and VI ( numerous trees like tributaries that Figs 2-5/ 9,10) represented the frequently received tufts of venous middle group forming the middle capillary network under the renal renal vein and draining the middle capsule.Multiple anastomoses were (hilar) zone. The remaining inter- visible between the inter-lobular lobar veins VII. VIII and IX (Figs 2-5 veins throughout the renal cortex / 11, 12, 13) constituted the caudal and near the surface of the kidney. group draining the corresponding 3rd The aforementioned data revealed of the ventral half of the kidney and that numerous anastomoses were joined to form the caudal renal vein. found in all renal parenchyma bet- Multiple longitudinal anastomoses ween the interlobar, the arcuate and were visible between the adjacent dorsal collateral veins as well as the interlobar veins (Fig 5/I, I, III) vertical anastomoses between throughout the renal medulla. dorsal collateral veins and the main ventral venous trunks as well as by Vv. Arcuata circular anastomosis around the The arcuate veins (Figs 2, 3, 6, 7, neck of the calyces minor forming 9/21) where connected to from the collar-shaped venous anastomoses interlobar veins in the vicinity of the (Fig 1/20). On that basis the renal corticomedullary junction either in venous system in the pig could not curved manner or at right angles or be segmented. as a collateral tributaries. The arcuate veins anastomosed with Discussion each other forming a sort of 7-8 arches. These longitudinal arcades The present study revealed that occur in different levels between the each kidney was served by single arcuate veins at the base of the principal renal vein connecting to medullary pyramids. The convex the caudal vena cava. In the cat aspect of the later arches received (Krahmer, 1966 and Webser, 1968), the interlobular veins. dog (Evans and Christensen, 1979) and lion (Abuzaid et al., 1993) both Vv. Interlobulares kidneys were drained by two renal The interlobular veins (Figs 2, 3, 6, veins. In the human kidney, any 7, 9 /22) were represented by additional vessel that drains the numerous vessels that follow a kidney into the vena cava should be flexuous course in radial direction considered as a normal variation though the cortical tissue. They and may be named as an additional

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Venous Architecture of pig kidney Farag,F.M.M. renal veins (Satyapal, 1993), or reported cranial and caudal renal “accessory renal veins” ( Hazirolan veins in 75% and cranial, inter- et al., 2011). Bergman et al. (1988) mediate and caudal ones in 25% of reported that the multiple renal the examined pig kidneys. On the veins are rare on the left side and contrary Oliveira (2008) mentioned common on the right. Fernandes et that the renal vein was formed by al. (2005) recorded triple right renal two trunks in 25%, three trunks in veins in human. From the point of 55%, four trunks in 15% and five view of this work the presence of ones in 5% of the examined bovine multiple renal veins could be kidneys. explained as 2nd order renal veins emptying directly into the vena cava Satyapal (1993) recorded the without forming a stem renal vein. systemic arrangement of the branching patterns of the human renal The slight cranial displacement of vein and concluded that there are the right renal vein compared to the five types; type (IA), comprised the left one that we observed in three two main tributaries, an upper and a dissected pig embryos is similar to lower primary one, type (IIA) added that described by Nickel et al. an intermediate one, type (IIIA) (1976) and Ghoshal et al. (1981) in included the two main tributaries the pig. However in two other with an independent additional specimens both renal veins joined renal vein, type (IB) was formed of the vena cava at the same level, the the two main tributaries with third same as has been recorded in the posterior one and finally type (IIB) dog and cat (Koch, 1976) and pig was formed of four tributaries; the (Vodenicharov and gulubova ,1995) upper, intermediate, lower and dorsal ones. On that basis the The current investigation revealed present study could be classed as that, the stem renal vein in the pig types (IA) and (IIA). arose from three tributaries: cranial, middle and caudal renal veins. In The present study revealed that this respect, in the same species, only the ventral half of the cranial Filho et al. (2008) recorded two and caudal thirds of the kidney were main trunks cranial and caudal in drained by the large veins rep- 88.53% and three trunks, cranial, resented by the cranial and caudal middle and caudal in 11.47% of the renal veins as well as their examined specimens. Similarly, Vo- interlobar veins. The dorsal half was denicharov and Gulubova (1995) drained by small dorsal collateral

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Venous Architecture of pig kidney Farag,F.M.M. veins that emptied by anastomoses the cases and added that these into the ventral set. Similar findings veins were relatively smaller than were also recorded by Filho et al. those of the human kidney and (2008) in the pig. On the other hand consequently the direct dorsal Oliveira (2008) reported dorsal and puncture of the dorsal surface of the ventral venous plexi in the cranial renal pelvis in the pig would not pole of the bovine kidney in 55% of results in important vascular compli- cases. Similarly, in the human cations as in the human (Clayman kidney (Sampaio and Aragao, 1990) et al.,1984). the superior caliceal group involved dorsal and ventral large veins in In accordance with Filho et al. 84.6% and the inferior caliceal (2008) in the pig, the three primary group in 50%, where large veins tributaries of the stem renal vein coursed parallel to the anterior and were arising from the union of posterior surfaces of the caliceal interlobar veins. On the other hand infundibula. Due to these ana- Vo-denicharov and gulubova (1995) tomical differences we realize that in the same animal reported that the dorsal infundibualar puncture in the primary division of the renal vein pig does not cause hazard to the was followed by secondary division veins and therefore, they don’t into prelobar veins before giving 9- cause back bleeding. On the 13 interlobar veins. The latter contrary, in the middle third, there authors added that in 50% of the were large veins in a close rela- examined specimens the cranial tionship to the ventral and dorsal renal vein was weaker and collected surface of the uretero-pelvic blood from the frontal third of the junction in 75% and 25% of the renal parenchyma while the caudal specimens respectively. Similarly renal vein drained the remaining Lee et al. (1988) and Clayman and two thirds. However, the present Picus (1988) recorded 91.16% and study explained the later obser- 3.28 in the corresponding region of vations by the origin of the middle the human kidney and recom- renal vein from the caudal renal mended that the deep incision of vein in nearly half the examined the uretero-pelvic junction to relieve specimens. its obstruction must be done The current investigations revealed laterally to avoid the risk of injury of that there were free anastomoses large veins. Filho et al. (2008) between the intrarenal veins. The observed large dorsal veins in the most frequent of these anas- uretero-pelvic region in 55.78% of

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Venous Architecture of pig kidney Farag,F.M.M. tomoses were found in the Ragab (1987) in the donkey longitudinal axis, in the medulla reported that the later veins were between the interlobar veins, at the limited to the part caudal to the hilus base of the medullary pyramids and therefore could be considered between the longitudinal arcades as diagnostic feature of that kidney. formed between the arcuate vein and also in the cortex between the interlobular veins. Similar findings References were recorded by (Sampaio and Aragao (1990) and Simpatico (1992) in human, Oliveira (2008) in Abuzaid. S.M., Gad, M.R. and bovine and Filho et al. (2008) in the Wally, Y.R. (1993): Renal pig kidney. It might be also added venous system of the lion that the vertical venous anas- (Panthera leo) a gross anato- tomoses in the pig kidney were mical description. Vet. Med. J. represented by the five directly Giza Vol. 41, No. 1, 131-135. emptying dorsal collateral veins into the interlobar veins as well as the Bergman, R.A., Thompson, numerous circular anastomoses S.A., Afifi, A.K. and Saadeh, which encircle the neck of the F.A. (1988): Compendium of calyces minor resembling the collars of man (Sampaio and human anatomy variation. Balti- Aragao,1990). These data showed more: Urbane & Schwarzenberg. that the renal venous system in the Christensen, G.C. (1952): Cir- domestic pig cannot be segmented. culation of the blood through the According to the present study no canine kidney. Am. J. Vet. Res., superficial veins could be detected 13, 236-245. in the pig kidney. In this respect Zimmermann (1972) and Abuzaid et Clayman, R.V. and Picus, D.D. al. (1993) recorded superficial (1988): Ureterorenoscopic endo- (capsular) veins in the kidney of the pyelotomy . Preliminary report. cat and lion respectively. Christen- Urol. Clin. North Am. 15:433. sen (1952) in the dog, Zimmermann (1972), in the cat reported stellate Clayman, R.V., Surya, V., veins that distributed all over the Hunter, D., Castaneda-Zuniga, entire surface of the kidney and W.R., Miller, R.P. and Coleman, were always visible. Osman and C. (1984): Renal vascular

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Venous Architecture of pig kidney Farag,F.M.M. complications associated with Hammond, L., Ketchum, j. and the percutaneous removal of Schwartz, B.F. (2004): A new renal calculi. J. Urol.132:228. approach to urology training: A laboratory model for percutan- Erap P.P. (2003): Percutaneous eous nephrolithotomy. J. Urol. renal surgery – new model for 172:1950. learning and training. Int. Braz. J. Urol. 29: 151. Hazirolan,T., Meryem, O. Turk- bey, B., Karaosmanoglu, A.D., Evans, H.E. and Christensen, Oguz , B.S. and Canyigit, M. G.C. (1979): Miller’s Anatomy of (2011). CT angiography of the the dog. Verlag. W.B. Saunders renal arteries and veins: normal CO. Philadelphia, London. anatomy and variant. Diagn. Fernandes, R.M.P., Conte, F.H. Interv. Radiol. ,17, 67-73. P., Favorito, L.A, Figueiredo, Jou,Y.C., Cheng, M.C., Sheen, M.A and Babinski M.A. (2005): J.H., Lin, C.T., and Chen, P.C. Triple right renal vein: An un- (2004): Electrocauterization of common variation. Int. J. Mor- bleeding points for percutaneous phol. 23 (3): 231-233. nephrolithotomy. J. Urology 64: Filho, H.J., Pereira-Sampaio, 443. M. A. , Favorito, L.A. and Sam- Kaouk, J.H., Gill, I.S., Desai, paio, F.J. (2008). Pig kidney ]: M.M., Banks, K.L., Raja, S.S., anatomical relationships bet- Skacel, M. et al (2003): Laparo- ween the intrarenal Venous scopic anatrophic nephrolitho- Arrangement and the kidney tomy feasibility study in a chronic collecting system. J. Urol. Vol. porcine model. J. Urol.; 169: 691. 179, 1627-1630. Koch, T. (1976): Lehrbuch der Ghoshal, N.G., Koch, T. and veterinär Anatomie 13 and III, 3- Popesko, P. (1981): The venous A, FLAGE, VEB Gustav Fischer drainage of the domestic Verlag, Jena. animals. W.B. Saunders Co. Philadelphia, London, Toronto, Krahmer,R. (1966): Beitrag Zum Sydney. Verhalten der Vena cava

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Venous Architecture of pig kidney Farag,F.M.M. caudalis and ihres visceralen intra-renal arteries and the zulluss-gebietes bie der Katze. kidney collecting system. Applied Anat. Anz. 118, 310-316. study for urological research and surgical training. J Urol. 172: Lee, W.J., Badlani, G.H., 2077–2081. Karlin, G.S. and Smith, A.D. (1988): Treatment of uretero- Sampaio, F.J. (1992): Anato- pelvic structures with percuta- mical background for nephron- neous pyelotomy. Experie-nce in sparing surgery in renal cell 62 patients. AJR Am J. carcinoma. J. Urol.147:999. Roentgenol 151:515. Sampaio, F.J. and Aragao, Nickel, R.A., Schummer, A. A.H. (1990): Anatomical rela- and Seifrle, E. (1976): Lehrbuch tionship between the renal der Anatomie der Haustiere, venous arrangement and the Band III, Veralg Paul, Parey, kidney collecting system. J. Urol. Berlin 144: 1089.

Oliveira, R.R. (2008): Bovine Sampaio, F.J., Pereira-Sampa- kidney: anatomical relationships io, M.A. and Favorito, L.A. between the intrarenal Venous (1998): The pig kidney as an Arrangement and the kidney endo-urologic model: anato-mic collecting system. Braz. J. contribution. J. Endourol. 1998, Morphol. Sci. 2008, Vol. 25 no. 12: 45. 1-4, p. 1-34. Satyapal, K.S. (1993): An ana- Osman, F.A. and Ragab, S.A. tomical exploration into the (1987): Anatomical studies on variable patterns of the venous the renal blood vessels of vasculature of the human kidney. donkey (Equus asinus). Assiut Doctoral Thesis, University of Vet. Med. J. Vol. 18, No. 56. Natal.

Pereira-Sampaio, M.A., Vodenicharov, A. Gulubova, M. Favorito, L.A. and Sampaio, (1995): Renal venous archi- F.J. (2004): Pig kidney: anato- tectonics in domestic swine. mical relationships between the Anat. Histol. Embryol. 24:149.

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Wesber, H. (1968): Ein Beitrag Zimmermann, E. T. (1972): Das Zum problem der Verdoppelung Blutgefassystem der Niere der der Vena cava caudalis bie der Katze (Felis catus L.). Diss. Vet. Katze.. Anat. Anz. 122: 491-495. Med. Zurich.

Legend for figs 1-9

1 V. renalis, 2 V. renalis cranialis, 3 V. renalis medius, 4 V. renalis caudalis, 5 V. interlobaris I, 6 V. interlobaris II, 7 V. interlobaris III, 8 V. interlobaris IV, 9 V. interlobaris V, 10 V. interlobaris VI, 11 V. interlobaris VII, 12 V. interlobaris VIII, 13 V. interlobaris IX, 14 V. collateralis dorsalis A, 15 V. collateralis dorsalis B, 16 V. collateralis dorsalis C, 17 V. collateralis dorsalis D, 18 V. collateralis dorsalis E, 19 V. collateralis dorsalis , 20 Collar shaped anastomoses, 21 Vv. Arcuata , 22 Vv. Interlobulares. A Extremitus cranialis, B Extremitus caudalis

Fig (1): A photograph showing cast of the intra-renal veins in the right kidney of the pig (ventral view).

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Fig (2): A photograph showing cast of the intra-renal veins in the right kidney of the pig (ventral view).

Fig (3): A photograph showing cast of the intra-renal veins in the right kidney of the pig (dorsal view).

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Fig (4): A photograph showing cast of the intra-renal veins in the right kidney of the pig (medial view). Note Arrangements of the veins into dorsal and ventral sets.

Fig (5): A photograph showing cast of the intra-renal veins in the left kidney of the pig (ventral view).

Each of the cranial and caudal renal veins was injected separately. Note: anastomoses between renal veins (black arrows I, II and III).

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Fig (6): Radiograph showing ventral view of the intra-renal veins in the right kidney of the pig.

Fig (7): Radiograph showing ventral view of the intra-renal veins in the right kidney of the pig.

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Fig (8): A radiograph showing ventral view of the intra-renal veins in the left kidney of the pig.

Fig (9): A radiograph showing ventral view of the intra-renal veins in the right kidney of the pig

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