FULL PAPER  Anatomy

Anatomical variation of arterial supply to the rabbit spleen Reona IKEGAMI1), Yoshimasa TANIMOTO1), Miori KISHIMOTO2) and Hideshi SHIBATA1)* 1)Laboratory 2)Laboratory

of Veterinary Anatomy, Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183–8509, Japan of Veterinary Imaging, Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183–8509, Japan

(Received 18 May 2015/Accepted 31 August 2015/Published online in J-STAGE 11 September 2015) ABSTRACT. The rabbit, which is widely used as an experimental animal and is also popular as a companion animal, has a flat and elongated spleen with the longitudinal hilus running along its visceral surface. The spleen receives via the hilus an arterial supply that is essential for splenic nutrition and normal functioning. However, the distribution and variation of the arteries to the spleen have not been studied in detail. This study investigated anatomical variations of splenic arterial supply in 33 New Zealand White rabbits with a colored latex injection into arteries. We also examined whether the length of the spleen correlated with the number of the splenic branches of the splenic artery. The splenic artery always arose as the first independent branch of the celiac artery and ran along the splenic hilus to usually provide 6 (range, 3 to 10) splenic branches to the spleen. There was a moderate correlation (R=0.6) between the number of splenic branches and the longitudinal length of the spleen. The splenic branches often arose as a trunk or trunks in common with short gastric arteries. The number of common trunk(s) was usually 1 (range, 0 to 4). The data showed that the pattern and number of arterial branches to the spleen varied according to the individual animal, suggesting that such variations should be considered when performing experimental and veterinary surgical treatments in rabbits. KEY WORDS: angiology, artery, macroscopic anatomy, rabbit, spleen

doi: 10.1292/jvms.15-0297; J. Vet. Med. Sci. 78(2): 199–202, 2016

The morphology of the spleen differs according to specific mammalian species [8, 15]. The spleen in the rabbit, which is widely used as an experimental animal and as a companion animal [1], is a flat and elongated organ with the longitudinal hilus running along its visceral surface [9]. The spleen receives an arterial supply through the branches of the splenic artery to support its nutrition and function, but the macroscopic description of the arterial pattern in rabbits often varies within the literature. For example, it is reported that the splenic artery arises as one of the trifurcated branches of the celiac artery [17] or as the first independent branch of the celiac artery [1, 2, 14]. In rodents, which are the closest relative to the lagomorph, the origin of the splenic artery varies in each species. For example, whereas in the rat [10], dormouse [18] and Mediterranean pine vole [20], the splenic artery usually arises as one of the trifurcated branches of the celiac artery, this artery usually arises as the first independent branch of the celiac artery in the hamster [7], muskrat [6], wood mouse [11] and degu [19] or as the second independent branch in the North American beaver [5]. Another pattern is seen in the guinea pig [4, 16], where the splenic artery usually arises as a common trunk with the left gastric artery. Furthermore, in most of the rodents above, the origin of the splenic artery sometimes varies depending on individuals within each species [4–7, 10, 11, 16, 18–20]. These studies in rodents suggest that there may be individual *Correspondence to: Shibata, H., Laboratory of Veterinary Anatomy, Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183–8509, Japan. e-mail: [email protected] ©2016 The Japanese Society of Veterinary Science

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License .

variations in the branching pattern of the splenic artery from the celiac artery in the rabbit. The splenic artery provides splenic branches that enter the spleen through its hilus [2, 17]. Although some ramification patterns of these branches have been described in a previous rabbit study by Bednářová and Malinovský [3], their descriptions are vague and inconclusive. For example, in their study [3], the pattern that they observed most frequently was that the splenic artery provided one ramus dorsalis and one ramus ventralis. However, they did not define each ramus definitively nor described its region of distribution. Furthermore, they mentioned that 2 to 10 branches issued from rami dorsalis and ventralis, but the branching pattern of these rami was not clarified. Therefore, the goal of the present study was to characterize more critically the anatomical variations of arterial supply to the rabbit spleen macroscopically via a colored latex injection. We also examined whether the length of the spleen correlates with the number of the splenic branches. MATERIALS AND METHODS We used 28 male and 5 female New Zealand White rabbits (weight, 2.5–3.0 kg), purchased from Tokyo Laboratory Animal Science Co (Tokyo, Japan). The present study was approved by the Research Ethical Committee for Animal Experimentation of the Tokyo University of Agriculture and Technology. The rabbits were sacrificed with intraperitoneal injection of sodium pentobarbital (60 mg/kg) and then perfused with fixative containing either 4% paraformaldehyde and 0.05% glutaraldehyde or 10% formalin. In the fixed cadaver in the dorsal position, some of their left ribs were removed to facilitate thoracic aortic incision, through which a cannula

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was inserted caudally to be injected with 3 to 8 ml of the colored latex (Neoprene latex 601A or 842A, Showa Denko, Kawasaki, Japan). After further fixation for more than 7 days in 10% formalin, we characterized the macroscopic arterial distribution to the spleen. Vernier calipers were used to measure the length of the spleen. RESULTS The rabbit spleen was located on the left caudolateral aspect of the stomach (Fig. 1A). The splenic artery arose as the first independent branch of the celiac artery in all the rabbits examined (Fig. 1B) and proceeded to the left toward the splenic hilus (Fig. 1B) that runs along the visceral surface of the spleen. Upon reaching the hilus, the splenic artery ran ventrally along the hilus to give off different numbers of the splenic branches to the spleen (Fig. 2) and then continued as the left gastroepiploic artery toward the greater curvature of the stomach (Figs. 1B and 2). Each splenic branch arose as either an independent branch of the splenic artery or as a trunk in common with a short gastric artery (This trunk will be simply referred to as “common trunk” hereafter). The first branch of the splenic artery was always a short gastric artery or the common trunk of a splenic branch with a short gastric artery (Fig. 2), but never a splenic branch. In cases in which the first splenic branch arose from the common trunk, the branch usually entered the hilus near the splenic dorsal extremity. In contrast, in cases where the first splenic branch arose independently from the splenic artery, the branch entered the hilus somewhat distant from the dorsal extremity (Fig. 2). The number of the splenic branches varied from 3 to 10 according to the specimen (Fig. 3A): 3 branches were present in 2 rabbits (6%), 4 branches in 3 rabbits (9%), 5 branches in 7 rabbits (21%), 6 branches in 8 rabbits (25%) (Fig. 2A and 2B), 7 branches in 6 rabbits (18%) (Fig. 2C and 2D), 8 branches in 4 rabbits (12%), 9 branches in 2 rabbits (6%) and 10 branches in 1 rabbit (3%). Furthermore, the number of the common trunk (s) of the splenic branches with short gastric arteries (Fig. 2A and 2B) varied from 0 to 4 (Fig. 3B): 0 common trunk in 5 rabbits (15%) (Fig. 2C and 2D), 1 common trunk in 12 rabbits (37%), 2 common trunks in 7 rabbits (21%), 3 common trunks in 6 rabbits (18%) and 4 common trunks in 3 rabbits (9%) (Fig. 2A and 2B). No correlation was observed between the number of the splenic branches/ common trunk(s) and the splenic arterial branching pattern. The dorsoventral length of the spleen varied from 31 to 68 mm, and 50% of the spleens were between 50 and 60 mm long (Fig. 4A). The length of the spleen correlated with the number of splenic branches (Fig. 4B) (R=0.60, P=0.008), but did not correlate with the number of the common trunk(s) of the splenic branches with short gastric arteries (R=0.19). There was no correlation between the number of splenic branches and the number of the common trunk(s) (R=0.12). There were no gender differences in the number of the splenic branches or common trunk(s), the pattern of the splenic arterial branching, or the dorsoventral length of the spleen.

DISCUSSION The present study characterizes in great detail the individual anatomical variations of the arterial supply to the spleen in the rabbit. In all rabbits examined, the splenic artery was the first independent branch of the celiac artery. However, Bednářová and Malinovský [3] demonstrated that not the splenic artery but the hepatic artery was the first branch in 1 out of 30 cases that they examined. This one rabbit is considered to be an exceptionally rare case, because other previous reports in the rabbit [1, 2, 14] consistently showed that the splenic artery was the first branch of the celiac artery, in agreement with our present results. In rodents, there are individual and/or species variations; the splenic artery is usually the first independent branch of the celiac artery in the Mediterranean pine vole [20], muskrat [6], wood mouse [11] and degu [19], frequently not the first independent branch in the dormouse [18], and never in the North American beaver [5] and guinea pig [4, 16]. We found the common trunk(s) of the splenic branches with short gastric arteries in 85% of the rabbits examined in this study (Fig. 3B). The number of the common trunk(s) varied from 0 to 4, with 1 common trunk (37%) being the most frequent. Abidu-Figueiredo et al. [1] did not describe such common trunks, whereas Bednářová and Malinovský [3] mentioned the existence of at least 1 “stem” in some of their cases, though their description was vague. These differences may be due to the possibility that Abidu-Figueiredo et al. used another breed of New Zealand rabbits, such as New Zealand Red [12], and Bednářová and Malinovský [3] used breeds other than the New Zealand White. In two studies in rodents (dormouse [18] and degu [19]), which are the closest relative to the lagomorph, it was reported that a trunk of the splenic artery gave off branches to the dorsal portion of the spleen and to part of the left visceral surface of the stomach. Similar trunks or “parent” branches that provide the splenic branches and short gastric arteries are also described in the dog [15]. These trunks in rodents and dogs correspond to the common trunk observed in the rabbit in the present study. In the chinchilla [13], one trunk, which is called the gastrosplenic artery, supplies the dorsal spleen and the greater curvature of the stomach and the other, which is called the splenic artery, supplies the central and the ventral spleen. However, these trunks branch off from the celiac artery at the same level. It is considered that these two trunks in the chinchilla may correspond to one common trunk of the splenic artery with a short gastric artery in the rabbit. The number of the splenic branches varied from 3 to 10 with 6 branches (25%) being the most frequent number among the rabbits examined in this study. However, AbiduFigueiredo et al. [1] studied 30 New Zealand rabbits (weight, 2.5 kg) and obtained different results in that the number of the splenic branches varies from 1 to 5 with 3 branches (33.3%) being the most frequent. In the rat, whose spleen is shaped similar to that of the rabbit [10], it is reported that the number of splenic branches was 5 to 8 [10]. This finding is similar to that from our study, wherein 76% of the rabbits have 5 to 8 splenic branches.

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Fig. 1. A: Photograph showing the rabbit spleen located on the left caudolateral aspect of the stomach. The left caudoventrolateral view. B: Photograph showing that the splenic artery arises as the first independent branch of the celiac artery. The left caudoventrolateral view. The stomach is reflected cranially. Abbreviations used in this and the following figure: a, artery; br, branch; du, duodenum; sp, spleen; and st, stomach.

Fig. 2. A: Photograph of a case with 6 splenic branches. Asterisks indicate common trunks of the splenic branches with short gastric arteries. B: Schematic drawing of A. C: Photograph of a case with 7 splenic branches and no common trunk. D: Schematic drawing of C.

We found a moderate correlation between the dorsoventral length of the spleen and the number of splenic branches (R=0.6, P=0.008). However, there was no correlation between the length and the number of the common trunk(s) or

between the number of splenic branches and the number of common trunk(s). Furthermore, the number of these branches and common trunk(s) does not relate to their branching pattern. Therefore, arterial variations demonstrated by the

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Fig. 3. A: Pie chart showing the incidence of the number of the splenic branches of the splenic artery. B: Pie chart showing the incidence of the common trunk(s) of the splenic branches with short gastric arteries.

Fig. 4. A: Pie chart showing the variation of the dorsoventral length of the spleen. B: Scatter diagram showing the correlation between the dorsoventral length of the spleen and the number of splenic branches (R=0.6, P=0.008).

present study should always be taken into account when performing experimental or veterinary surgery in rabbits. REFERENCES 1. Abidu-Figueiredo, M., Xavier-Siva, B., Cardinot, T. M., Babinski, M. A. and Chagas, M. A. 2008. Celiac artery in New Zealand rabbit: anatomical study of its origin and arrangement for experimental research and surgical practice. Pesqui. Vet. Bras. 28:

237–240. [CrossRef] 2. Barone, R., Pavaux, C., Blin, P. C. and Cuq, P. 1973. Atlas d’Anatomie du Lapin (translated into Japanese by Mochizuki, K.), Gakusosha, Tokyo. 3. Bednářová, Z. and Malinovský, L. 1988. Ramification of the coeliac artery in the domestic rabbit (Oryctolagus cuniculus f. domestica). Scr. Med. (Brno) 61: 17–34. 4. Bednářová, Z. and Malinovský, L. 1990. Variability of branching of the a. coeliaca (truncus coeliacomesentericus) in the guinea pig (Cavia aperea f. porcellus). Folia Morphol. (Praha) 38: 382–395. [Medline] 5. Bisaillon, A. and Bhérer, J. 1979. Gross anatomy of the arterial supply of the stomach of the North American beaver (Castor canadensis). Acta Anat. (Basel) 104: 79–85. [Medline] [CrossRef] 6. Bisaillon, A., Grenier, A. and Bousquet, R. 1988. Arterial blood supply to the stomach of the muskrat (Ondatra zibethicus). Anat. Histol. Embryol. 17: 7–11. [Medline] [CrossRef] 7. Bivin, W. S., Olsen, G. A. and Murray, K. A. 1987. Morphophysiology. pp. 10–41. In: Laboratory Hamsters. (Van Hoosier, G. L. Jr. and McPherson, C. W. eds.), Academic Press, Orlando. 8. Evans, H. E. and de Lahunta, A. 2013. Miller’s Anatomy of the Dog, 4th ed., Elsevier, St. Louis. 9. Harcourt-Brown, F. 2002. Textbook of Rabbit Medicine, Butterworth-Heinemann, Oxford. 10. Hebel, R. and Stromberg, M. W. 1986. Anatomy and Embryology of the Laboratory Rat, BioMed Verlag, Wörthsee. 11. López-Fuster, M. J. and Ventura, J. 1992. Arrangement of the branches of the aorta abdominalis in the wood mouse (Apodemus sylvaticus). Anat. Histol. Embryol. 21: 146–151. [Medline] [CrossRef] 12. Meredith, A. 2006. General biology and husbandry. pp. 1–17. In: BSAVA Manual of Rabbit Medicine and Surgery, 2nd ed. (Meredith, A. and Flecknell, P. eds.), British Small Animal Veterinary Association, Gloucester. 13. Özdemir, V., Çevik Demirkan, A. and Akosman, M. S. 2013. Subgross and macroscopic investigation of the coeliac artery in the chinchilla (chinchilla lanigera). Folia Morphol. (Warsz) 72: 258–262. [Medline] [CrossRef] 14. Popesko, P., Rajtova, V. and Horak, J. 2002. A Colour Atlas of Anatomy of Small Laboratory Animals. Volume 1, Saunders, London. 15. Schummer, A., Wilkens, H., Vollmerhaus, B. and Habermehl, K.H. 1983. The Anatomy of the Domestic Animals. Volume 2. The Circulatory System, the Skin, and the Cutaneous Organs of the Domestic Mammals, Verlag Paul Parey, Berlin. 16. Shively, M. J. and Stump, J. E. 1975. The systemic arterial pattern of the guinea pig: the abdomen. Anat. Rec. 182: 355–366. [Medline] [CrossRef] 17. Tsuzaki, K. 1935. The Anatomy of the Experimental Animals. Domestic Rabbit (in Japanese), Kanehara Shoten, Tokyo. 18. Ventura, J. and López-Fuster, M. J. 1994. The arterial system of the abdominal viscera and the pelvis of the dormouse, Eliomys quercinus (Gliridae, Rodentia). Ann. Anat. 176: 327–331. [Medline] [CrossRef] 19. Ventura, J., Gispert, E. and López-Fuster, M. J. 1996. Arterial vascularization of the abdominal and pelvic regions in the degu, Octodon degus (Rodentia, Octodontidae). Ann. Anat. 178: 285–291. [Medline] [CrossRef] 20. Ventura, J., López-Fuster, M. J. and Gispert, E. 1995. Blood supply to the abdominal and pelvic regions in the Mediterranean pine vole, Microtus duodecimcostatus (Rodentia, Arvicolidae). Anat. Histol. Embryol. 24: 133–137. [Medline] [CrossRef]

Anatomical variation of arterial supply to the rabbit spleen.

The rabbit, which is widely used as an experimental animal and is also popular as a companion animal, has a flat and elongated spleen with the longitu...
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