Casteleyn, Christophe

Cornillie, Pieter

Van Cruchten, Steven

Van Ginneken, Christa

Ghent University Academic Bibliography

 1 Left retrocaval ureter around the ipsilateral limb of a double 1 caudal vena cava in a cat 2  3  4 C. Casteleyna, P. Cornillieb, S. Van Cruchtena and C. Van Ginnekena 5  6  7 a Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty 8 of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, 9 Universiteitsplein 1, B-2610 Wilrijk, Belgium 10 b Department of Morphology, Faculty of Veterinary Medicine, Ghent University, 11 Salisburylaan 133, B-9820 Merelbeke, Belgium 12  13  14  15 Correspondence to: Christophe Casteleyn 16 christophe.casteleyn@uantwerpen.be 17 Tel.: +32 3 265 282118  2 Summary 19 Necropsy of an adult, neutered male cat, which was euthanized due to its FIV-positive status, 20 demonstrated the presence of a left retrocaval ureter that was entrapped around the left limb 21 of a double caudal vena cava. These associated anomalies originate from the complex 22 embryofoetal development of the caudal vena cava. Since no clinical signs had been reported 23 and no gross lesions related to this anomaly were observed, this manifestation should be 24 considered as a mere anatomical variation. 25  26 Keywords: Double caudal vena cava; retrocaval ureter; cat 27  3 An adult, neutered male cat (Felis catus) was euthanized after being tested positive for 28 FIV (feline immunodeficiency virus). The cadaver was presented at the Department of 29 Veterinary Sciences of the University of Antwerp for educational purposes. No gross 30 macroscopic lesions potentially associated with FIV positivity were found. However, the cat 31 presented a double caudal vena cava. More specifically, the left and right caudal vena cava 32 merged only at the level of the first lumbar vertebra to form a single vessel. The left and right 33 caudal vena cava individually drained the ipsilateral common iliac veins. No anastomoses 34 were found between the left and right counterparts at the level of the iliac veins, nor between 35 any other segment of the double caudal vena cava. Just prior to its confluence with its 36 contralateral part, the left caudal vena cava crossed the abdominal aorta ventrally (Fig. 1). 37 The complex embryofoetal development of the caudal vena cava lies at the basis of the 38 observed vascular anomaly. For years, the supracardinal model that was published (for the 39 cat) in 1920 by Huntington and McClure was considered the gold standard. This model that is  40 applied in both human and veterinary embryology states that the right-sided counterparts of 41 three pairs of embryonic veins (i.e. supracardinal, subcardinal and caudal cardinal veins) form 42 the abdominal part of the caudal vena cava by means of fusion, anastomosis and asymmetric 43 vascular degeneration during prenatal life (Huntington and McClure, 1920; Butler, 1927; 44 Cornillie and Simoens, 2005; Cornillie et al., 2006; Hyttel, 2010; Sadler, 2012). 45 However, a recent study revisiting the development of the inferior vena cava and vena 46 azygos by means of three-dimensional reconstructions of human embryos (Hikspoors et al., 47 2014) has revealed various inaccuracies in the supracardinal system of Huntington and 48 McClure (1920). All dorsal veins, formerly indicated as the supracardinal veins, have to be 49 considered as actual segments of the caudal cardinal system that gradually adopts a different 50 topography due to allometric growth of surrounding organs and tissues. What is important for 51 the present case is that, according to these recent insights, two paired longitudinal channels 52  4 can be found in the region of the kidneys, namely both caudal cardinal veins, which course at 53 the dorsomedial side of the kidneys, and the caudal extensions of the subcardinal veins, which 54 also run medially but ventral to the kidneys. 55 At the pelvic inlet, just caudal to the bifurcation of the aorta into the umbilical arteries, 56 these four veins are united in a huge anastomosis. At a certain point during development the 57 caudal cardinal venous segments draining into the subcardinal anastomosis at the 58 craniomedial poles of the kidneys, the infrarenal segments of the subcardinal veins collecting 59 and interconnecting the left and right common iliac veins, and tributaries of both venous 60 systems form a vascular ring around the ipsilateral kidney and ureter (Cornillie and Simoens, 61 2005; Hikspoors et al., 2014). This complex venous configuration evolves from a bilateral 62 symmetric system to a single, right-sided vein, in a process during which the left-sided 63 counterparts of all aforementioned veins gradually disappear (Cornillie and Simoens, 2005) 64 (Fig. 2). The presence of a double caudal vena cava is therefore considered to result from the 65 persistence of the left-sided venous segments, in combination with the absence of the 66 aforementioned iliac anastomosis (Bass et al., 2000; Cornillie, 2008). 67 Moreover, careful dissection during necropsy revealed another curiosity. The left 68 ureter was entrapped by the left (limb of the) caudal vena cava, a condition known as 69 retrocaval or circumcaval ureter (Gramegna et al., 2003). It slightly deviated towards the 70 midline to cross the left caudal vena cava dorsally, at the level of the fifth lumbar vertebra. 71 The left ureter resumed its more lateral course towards the urinary bladder after emerging 72 between the vein and the left psoas musculature. The right ureter presented a normal course 73 along the right psoas muscles (Fig. 3). 74 A rare case of retrocaval ureter in an intact male cat was reported in 2006 by Cornillie 75 and co-workers. This cat, however, presented a right retrocaval ureter associated with a single 76 caudal vena cava. The recently gained insights into the development of the infrarenal part of 77  5 the caudal vena cava allow formulation of the following hypothesis on the origin of a 78 retrocaval ureter. The basis is that the infrarenal segment of the subcardinal vein, which forms 79 the ventral branch of the circumureteric vascular ring, persists instead of the dorsally located 80 caudal cardinal vein. When the subcardinal vein contributes in the formation of the caudal 81 vena cava, it will cross the ureter ventrally and sweep it along its migratory path towards the 82 midline. This results in the medial deviation and entrapment of the ureter between the caudal 83 vena cava and psoas musculature. In our case with occurrence of a left retrocaval ureter 84 associated with a double caudal vena cava, it is hypothesized that this occurred on the left 85 side. More specifically, the infrarenal part of the left limb of the caudal vena cava was formed 86 by the persisting infrarenal segment of the subcardinal vein that runs ventral to the left ureter, 87 while the right limb was formed by the caudal cardinal vein that runs dorsal to the right ureter 88 (Fig. 4). 89 According to an extended study performed by Bélanger and co-workers (2014), who 90 examined the carcasses of 301 cats, a right retrocaval ureter is a rather common anatomic 91 variation. It was seen in 28% of the examined carcasses. Far more unique is the presence of a 92 left retrocaval ureter, having a prevalence of 1%. The presence of a double caudal vena cava 93 without entrapment of one or both ureters is seldom seen (0.7%). The combination of the 94 vascular and urinary variations is more typical as it has been observed in approximately 5% of 95 the examined carcasses. The combination of a left retrocaval ureter and a double caudal vena 96 cava was only observed in one female cat (Bélanger et al., 2014). So, this case report is the 97 first to describe these findings in a male cat.  98 The clinical relevance of the presented anomalies is unknown since no gross 99 macroscopic lesions were observed and no clinical signs had been reported. Nevertheless, it is 100 likely that cats with retrocaval ureters are more susceptible to ureteral obstruction and 101 consequently hydronephrosis. The former can be the result of the external pressure exerted on 102  6 the ureter by the caudal vena cava that retracts the ureter to the midline (Cornillie et al., 103 2006). Moreover, humans that develop kidney stones may suffer from obstructing uroliths 104 that cannot pass the ureter where it sweeps around the caudal vena cava to flow to the urinary 105 bladder (Soundappan and Barker, 2004). In cats, the pathogenesis of urolithiasis is different 106 from that in humans as cats are more prone to develop lower urinary tract disease. This is 107 characterized, amongst others, by the formation of urinary bladder stones and the potential 108 obstruction of the urethra (Lund et al., 2013).  109 In summary, retrocaval ureter(s) and/or a double caudal vena cava in cats are rarely 110 observed during necropsy. Since no clinical signs have yet been associated with these 111 anomalies, they should be considered as mere anatomical variations. 112  113 Conflict of interest statement: The authors have no conflict of interest to report. 114  115 References 116 Bass JE, Redwine MD, Kramer LA, Huynh PT, Harris JH (2000) Spectrum of congenital 117 anomalies of the inferior vena cava: cross-sectional imaging findings. Radiographics, 20, 118 639-652. 119 Bélanger R, Shmon CL, Gilbert PJ, Linn KA (2014) Prevalence of circumcaval ureters and 120 double caudal vena cava in cats. American Journal of Veterinary Research, 75, 91-95. 121 Butler EG (1927) The relative role played by the embryonic veins in the development of the 122 mammalian vena cava posterior. American Journal of Anatomy, 39, 267-353. 123 Cornillie P (2008) Development of the caudal vena cava in the pig embryo: a three-124 dimensonal angiogenic model. PhD Thesis, Ghent University. 125 Cornillie P, Baten T, Simoens P (2006) Retrocaval ureter in a cat. The Veterinary Record, 126 159, 24-25. 127  7 Cornillie P, Simoens P (2005) Prenatal development of the caudal vena cava in mammals: 128 review of the different theories with special reference to the dog. Anatomia, Histologia, 129 Embryologia, 34, 364-372. 130 Gramegna V, Madaro A, Pellegrini F, Capizzi S, Romano O, et al. (2003) A rare case of 131 retrocaval ureter associated with persistent left vena cava. Urologia Internationalis, 70, 132 337-338. 133 Hikspoors JPJM, Soffers JHM, Mekonen HK, Cornillie P, Köhler SE et al. (2014). 134 Development of the infrahepatic inferior caval and azygos venous systems in human. 135 Journal of Anatomy (in press). 136 Huntington GS, McClure CFW (1920) The development of the veins in the domestic cat 137 (Felis domestica) with especial reference, 1) to the share taken by the supracardinal veins 138 in the development of the postcava and azygos veins and 2) to the interpretation of the 139 variant conditions of the postcava and its tributaries, as found in the adult. The Anatomical 140 Record, 20, 1-30. 141 Hyttel P (2010) Development of the blood cells, heart and vascular system. In: Essentials of 142 Domestic Animal Embryology, 1st Edit., P Hyttel, F Sinowatz, M Vejlsted, Eds., Elsevier, 143 Oxford, pp. 182-207. 144 Lund HS, Krontveit RI, Halvorsen I, Eggertsdóttir AV (2013) Evaluation of urinalyses from 145 untreated adult cats with lower urinary tract disease and healthy control cats: Predictive 146 abilities and clinical relevance. Journal of Feline Medicine and Surgery, 15, 1086-1097. 147 Sadler TW (2012) Cardiovascular system. In: Langman’s Medical Embryology, 12th Edit., 148 TW Sadler, Ed., Lippincot Williams & Wilkins, Philadelphia, 162-200. 149 Soundappan SVS, Barker AP (2004) Retrocaval ureter in children: a report of two cases. 150 Pediatric Surgery International, 20, 158-160. 151  8 Figure legends 152 Fig. 1. Ventral view of the opened abdominal cavity in a necropsied neutered male cat 153 demonstrating the presence of a left caudal vena cava (l cvc) and a right caudal vena cava (r 154 cvc). The left ureter (arrows) is entrapped by the former vessel. ll = left lung, li = liver, st = 155 stomach, sp = spleen, l rv = left renal vein, lk = left kidney, cd = colon descendens, j = 156 jejunum, ub = urinary bladder, fh = femoral head. 157  158 Fig. 2. Ventral schematic views of a human embryo (L = left side, R = right side) showing the 159 development of the caudal vena cava (after Hikspoors et al., 2014). First (left image), a 160 vascular ring around each kidney and ureter is formed by the caudal cardinal venous segments 161 (1: I and IV) that drain into the subcardinal anastomosis (a and b) at the craniomedial poles of 162 the kidneys (2), the infrarenal segments of the subcardinal veins (3: II and III) that collect (c 163 and d) and interconnect (e) the left and right common iliac veins, and tributaries of both 164 venous systems. The paired subcardinal vein anastomoses in the ventral midline (f). 165 Subsequently (right image), the infrarenal part of the caudal vena cava is formed by the 166 interconnection of the left and right common iliac veins (e). The renal part is made of the 167 right-sided caudal cardinal vein (I), whereas the suprarenal segment is formed by the right 168 side of the regressing anastomosis (f). The renal veins originate from the cranial anastomoses 169 between the caudal cardinal and subcardinal venous systems (a and b). 170  171 Fig. 3. Ventral view of the abdominal cavity of the same cat as in Fig. 1. The structures of 172 interest have been dissected to clearly show the retrocaval position of the left ureter. The 173 kidneys have been removed and the urinary bladder was incised to investigate the potential 174 presence of hydronephrosis and urolithiasis, respectively. cvc = caudal vena cava, l cvc = left 175  9 caudal vena cava, r cvc = right caudal vena cava, lu = left ureter, pm = psoas muscles, aa = 176 abdominal aorta, ru = right ureter, fh = femoral head, ub = urinary bladder. 177  178 Fig. 4. Schematic representation of the formation of a left retrocaval ureter in the presence of 179 a double caudal vena cava. When the left limb of the caudal vena cava (l cvc) is formed by the 180 persisting subcardinal vein (III), it will cross the ureter ventrally and entrap it while making 181 the anastomosis with the caudal cardinal vein (d), which is located dorsal to the ureter, at the 182 pelvic inlet. The absence of a right retrocaval ureter is explained by the formation of the right 183 limb of the caudal vena cava by the right caudal cardinal vein (a, I and c) that runs dorsal to 184 the ureter. lk = left kidney, lu = left ureter, rk = right kidney, ru = right ureter, cvc = caudal 185 vena cava, r cvc = right caudal vena cava. 186   187 

Left retrocaval ureter around the ipsilateral limb of a double caudal vena cava in a cat

Abstract: Necropsy examination of an adult neutered male cat, which was humanely destroyed as it had feline immunodeficiency virus (FIV) infection, demonstrated the presence of a left retrocaval ureter that was entrapped around the left limb of a double caudal vena cava. These associated anomalies originate from the complex embryofetal development of the caudal vena cava. Since no clinical signs had been reported and no gross lesions related to this anomaly were observed, this manifestation should be simply considered as an anatomical variation

Cornillie, P.

van Ginneken, Christa

Institutional Repository Universiteit Antwerpen

https://biblio.ugent.be/publication/5836214/file/5836230

Left retrocaval ureter around the ipsilateral limb of a double caudal vena cava in a cat

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Ghent University Academic Bibliography

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