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Published in final edited form as: J Vasc Interv Radiol. 2019 Jun 13;30(12):2009–2015.e1. doi: 10.1016/j.jvir.2019.03.005

Angiographic Atlas of the Visceral Vascular Anatomy in Translational Rat Models

Donghua Shi 1,2,¥, Ryan M Kiefer 1,2, Hideyuki Nishiofuku 4, Andrea Cortes 5, Gregory J Nadolski 1,2, Stephen J Hunt 1,2, Rony Avritscher 5, Terence P F Gade 1,2,3,*
PMCID: PMC7193740  NIHMSID: NIHMS1531825  PMID: 31202678

Abstract

Purpose:

To characterize the angiographic and cross sectional imaging anatomy of the rat visceral vasculature in two translational models.

Materials and Methods:

Animal studies were conducted in accordance with institutional guidelines and approval of the Institutional Animal Care and Use Committees. Retrospective review of digital subtraction arteriography was performed in 65 Wistar and 50 Sprague-Dawley male rats through a left common carotid artery or right common femoral artery approach. Magnetic resonance imaging of the abdomen was performed on these rats to correlate imaging modalities.

Results:

Aortography was performed in three locations including cranial to the celiac artery, cranial to the renal arteries, and cranial to the caudal (inferior) mesenteric artery enabling characterization of the visceral branch arteries in all 65 Wistar rats. Selective arteriography of first, second and/or third order branch vessels of the aorta was performed allowing characterization of normal and variant anatomy. Dedicated selective arteriography of the celiac artery was performed in 65 Wistar and 10 Sprague-Dawley rats, of the common hepatic artery in 65 Wistar and 50 Sprague-Dawley rats, and of the cranial mesenteric artery in 43 Wistar rats. Magnetic resonance imaging enabled correlation with the lobar and portal venous anatomy.

Conclusions:

Analysis of arteriography and magnetic resonance imaging in these rat models will provide translational researchers with anatomic details needed to develop new endovascular protocols for small animal research in interventional radiology.

Keywords: Visceral angiography, translational rat model, vascular anatomy

INTRODUCTION

Minimally invasive endovascular procedures to treat diseases of the abdominal viscera, and particularly the liver, have continued to grow over the past several decades increasing the diagnostic and therapeutic options available for patients [1,2]. To support the growth of minimally invasive techniques for hepatic intervention, numerous translational models of liver cancer have been developed in an effort to improve the efficacy of hepatic interventions while reducing their morbidity [3]. While small animal models have been limited in some applications by their size, prior research has shown that endovascular techniques are successful in rat models [4,5]. .. Additionally, the wide range of modern cellular and molecular biology research platforms available for small animal models have become essential tools for accurately characterizing the mechanistic underpinnings of biological processes relevant to the field of interventional oncology [6]. Together, the growing ability to perform interventional techniques in small animal models with the robust biologic testing available for rodents make them appealing models for studying various pathologies. Further knowledge of the angiographic anatomy and variations of the rat abdominal arteries as well as the correlation with cross-sectional imaging anatomy will facilitate the application of rodent models for research on endovascular therapies beyond oncology.

The gross anatomy of the rodent abdominal vasculature has been described previously in the veterinary literature using vivisection or corrosion casts to delineate the origin, course and sizes of the celiac artery as well as the portal vein and intrahepatic vasculature [7–14]. In addition, the cross-sectional anatomy of the hepatic vasculature has been delineated using computed tomography (CT) with three-dimensional reconstructions of liver parenchymal units and intrahepatic microvasculature[15–17]. Despite its central role in endovascular interventions, the angiographic anatomy of the rat abdominal vasculature on fluoroscopy has not been completely described.

To address this deficiency, studies to delineate the angiographic anatomy of the rat abdominal vasculature, with particular attention to the major branch vessels of the aorta and celiac artery, were performed and correlated the arterial anatomy with the lobar and portal venous anatomy of the liver on magnetic resonance imaging (MRI).

MATERIALS & METHODS

Animal Model

Animal studies were conducted in accordance with institutional guidelines and approval of the Institutional Animal Care and Use Committees. Angiographic and MR images were retrospectively analyzed from a cohort of 65 male Wistar rats (Charles River Laboratories, Wilmington, MA) bearing diethylnitrosamine-induced hepatocellular carcinomas which were acquired as part of another study and from a cohort of 91 Sprague-Dawley rats (Charles River Laboratories, Wilmington, MA), of which, 50 were inoculated with N1S1 Novikoff hepatocellular carcinomas. All rats from the parallel protocols with available fluoroscopic studies were included in this observational study. Animal husbandry was performed as described previously.[4, 5] The median weight of the Wistar cohort was 403 grams (range: 301–496g). The median weight of the Sprague-Dawley cohort was 318 grams (range: 227–477g).

Arteriography

Anesthesia was administered using inhaled isoflurane (2%) with core body temperature monitored using a rectal temperature probe and maintained at 37°C using a circulating water blanket as previously described for all animals.[4] Arterial access for Wistar rats was performed from a left common carotid (LCCA, n=15) or right common femoral approach (RCF, n=50) as described previously.[4,5] In brief, access to the right common femoral artery was achieved using a small incision to expose the femoral artery and direct arterial puncture with a 26-gauge needle was performed after which a 0.014” guidewire was inserted to direct a 1.5F microcatheter. Access to the LCCA was achieved similarly using an incision for exposure followed by puncture with a 20-gauge needle and introduction of a 0.014” guidewire after which a 1.5F (Wistar) or 1.6F (Sprague-Dawley) microcatheter was introduced. A LCCA access was used for all Sprague-Dawley rats (n=91). The abdomen was centered between the image detector and x-ray tube of an AngioStar Plus Imaging System (Siemens, Malvern, Pennsylvania). Preshaped (J or 90°) microcatheters (Excelsior SL-10 Microcatheter, Stryker, Kalamazoo, MI, USA) custom modified to 30 cm in length with the catheter hub replaced was introduced into the LCCA or RFA with the aid of a coaxially inserted 0.014-inch guide wire (Transend, Stryker). Following the completion of the procedure, the arteriotomy and incision were closed as described previously.[4,5 All procedures were performed by fellowship trained interventional radiologists.

Nonselective arteriography was conducted in all Wistar rats and performed in three approximate locations: 1 cm cranial to the celiac artery, 1 cm cranial to the renal arteries, and 1 cm cranial to the caudal mesenteric artery. These locations were approximated using bony landmarks, with the celiac artery originating in the area of L1–L2 intervertebral disc space, the renal arteries in the area of L3–L4 intervertebral disc space, and the caudal mesenteric artery in the area of L5–L6 intervertebral disc space. Selective arteriography was conducted in both Wistar and Sprague-Dawley rats and performed by advancing the catheter into the ostium of the target branch vessel. First-order branches are defined as those arteries directly branching off the aorta, including the celiac, cranial mesenteric, renal, caudal mesenteric, and iliac arteries. The acquired fluoroscopic images were correlated with the gross anatomy and cross-sectional imaging descriptions in the literature to confirm appropriate identification.[7–10, 12, 13, 18] Digital subtraction arteriography (DSA) was performed though the hand injection of iopamidol contrast medium (Isovue® 370, 0.3mL; Bracco Diagnostics, Inc., Monroe Township, NJ).

Magnetic Resonance Imaging

All Wistar rats underwent magnetic resonance imaging prior to fluoroscopic evaluation as has been previously described.[4] T1-weighted images were acquired in the axial plane with 70 × 70 mm field of view, 256 × 256 matrix size, 2 mm slice thickness, 0 interslice gap, 8 signal averages, and TR of 250 ms both pre- and post-contrast administration with 30% gadolinium in saline injected via tail vein catheterization. Respiratory gated, fat-saturated T2-weighted images were acquired in the axial and coronal planes with 70 × 70 mm field of view, 256 × 256 matrix size, 2 mm slice thickness, 0 interslice gap, 8 signal averages, and TR minimized. All rats that underwent imaging were anesthetized using inhaled isoflurane to maintain adequate sedation with a respiratory rate around 40 breaths per minute and homeostatic core temperature maintained with circulated warm air through the magnet bore. All imaging was acquired using a Varian 4.7-tesla 40-cm horizontal bore MR spectrometer with a 25 gauss/cm gradient tube interfaced to a Varian DirectDrive console (Agilent Technologies, Santa Clara, California).

Image Analyses

Angiographic and MR images were analyzed using OsiriX software (Pixmeo SARL, Bernex, Switzerland). All images were analyzed by board-certified, fellowship-trained interventional radiologists, each with at least 8 years working with the respective models.

RESULTS

Nonselective Arteriography

Aortography was performed in rats as indicated in Table 1. Aortography performed with the catheter positioned 1 cm cranial to the celiac artery was successful in identifying the ostium of the celiac and cranial (superior) mesenteric arteries in all 65 rats (Fig. 1A). The ostia of the bilateral renal arteries were identified in 95% (62/65) of Wistar rats (Fig. 1B). The ostium of the right renal artery was located cranial to the ostium of the left renal artery in 95% (59/62) of Wistar rats where both renal ostia were identified (Fig. 1B).

Table 1.

Aortography

Selectivity Anatomic Position Number of Rats
Nonselective aortography 1cm Cranial to Celiac Artery 65 Wistar, 0 Sprague-Dawley
1cm Cranial to Renal Arteries 65 Wistar, 0 Sprague-Dawley
1cm Cranial to Caudal Mesenteric Artery 21 Wistar, 0 Sprague-Dawley
Selective arteriography Celiac Artery 65 Wistar, 10 Sprague-Dawley
Common Hepatic Artery 65 Wistar, 50 Sprague-Dawley
Proper Hepatic Artery 65 Wistar, 46 Sprague-Dawley
Cranial Mesenteric Artery 43 Wistar, 0 Sprague-Dawley
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Figure 1.

Figure 1

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Nonselective aortography with catheter tip placed in thoracic aorta (A), 1 cm cranial to the celiac (B), 1 cm cranial to the renal arteries (C) and 1 cm cranial to the caudal mesenteric (D). A: Aorta; IcA: Intercostal Artery; CT: Celiac Trunk; R: Renal Artery (Right); CrM: Cranial Mesenteric Artery; RSA: Right Spermatic Artery; LSA: Left Spermatic Artery; CaM: Caudal Mesenteric Artery; HPA: Hepatic Proper; GDA: Gastroduodenal; CHA: Common Hepatic; LGA: Left Gastric; SA: Splenic; RRA: Right Renal; LRA: Left Renal; IlA: Iliolumbar; RIA: Right Iliac; LIA: Left Iliac; MSA: Median Sacral; EPA: External Pudendal; CEA: Caudal Epigastric; RK: right kidney; ICA: ileocolic.

Aortography performed with the catheter positioned cranial to the renal arteries demonstrated that the most caudal renal artery branched caudal to the cranial mesenteric artery in 97% (63/65) of Wistar rats (Fig. 1B). The right renal artery branched caudolaterally off the aorta and continued further craniolaterally in 58 rats, directly laterally in 3 rats and branched only cranially in 4 rats. The left renal artery branched caudolaterally off the aorta and continued further craniolaterally in 55 rats, directly laterally in 6 rats and branched only cranially in 4 rats.

Aortography was performed with the catheter positioned 1 cm cranial to the caudal mesenteric artery and opacified the caudal (inferior) mesenteric artery and iliolumbar arteries in 21 rats (Fig. 1D). The caudal mesenteric artery branched off the aorta in a leftward direction in 71% (15/21) of rats and its origin was not clearly observed in the remaining 6. The ostium of the caudal mesenteric artery was identified immediately caudal to the left renal artery in all rats in which it was identified. The left colic artery was identified as a branch of the caudal mesenteric artery in 9 rats while the cranial rectal artery was not identified. DSA of the caudal mesenteric artery also demonstrated the bilateral spermatic arteries in 17 rats with the left and right spermatic arteries also observed to branch off the aorta at different levels (Fig.1A–C). Although not a first order branch of the aorta, the external pudendal/caudal epigastric arteries were noted bilaterally in 11 rats (Fig. 1C–D). Non-selective arteriography was not routinely performed in the Sprague-Dawley rats.

Selective Arteriography

The celiac artery was successfully selected in all 115 rats. Dedicated celiac arteriography was performed in all 65 Wistar rats and 10 Sprague-Dawley rats (Fig. 2A). The common hepatic, left gastric and splenic arteries were identified through this injection in all 65 Wistar and the 10 Sprague-Dawley rats (Fig. 2B). The splenic and left gastric arteries were selectively catheterized in only 13 animals, as they were not relevant to primary study. The common hepatic artery was successfully selected in all 115 rats (Fig. 2C). Selection and DSA of the common hepatic artery identified third-order branches of the aorta including the proper hepatic artery and the gastroduodenal artery in all 115 rats. The cranial pancreaticoduodenal artery was identified in 46% (30/65) of Wistar and 46% (23/50) of Sprague-Dawley rats, and the right gastroepiploic artery was identified in 18% (12/65) of Wistar and 44% (22/50) of Sprague-Dawley rats. The proper hepatic artery was successfully cannulated in 92% (46/50) of Sprague-Dawley rats. In addition, intrahepatic arterial branches were identified upon contrast injection in the common hepatic artery in all 115 rats (Fig 2C). The hepatic arteries were easily distinguished from the right gastric and right gastroepiploic arteries during contrast administration by observing the flow of contrast to the liver parenchyma. Selection and DSA of the splenic artery demonstrated its division into two branches in 8 rats, whereas, a single splenic artery was identified in 5 rats (Fig. 2D). The splenic hilar vessels were identified in 13 rats; however, short gastric arteries were not identified.

Figure 2.

Figure 2

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Selective arteriography with catheter tip inserted into celiac trunk (A), left gastric artery (B), common hepatic artery (C) and splenic artery (D). CHA: common hepatic; SA: splenic; LGA: left gastric; GDA: gastroduodenal; HPA: hepatic proper; RHA: right hepatic; LHA: left hepatic; GeA(R): right gastroepiploic; PdA(Cr): cranial pancreaticoduodenal; RGA: right gastric; RMHB: right median hepatic branch; RLHB: right lateral hepatic branch; LLHB: left lateral hepatic branch; LMHB: left median hepatic branch; CrB: cranial branch of splenic; CaB: caudal branch of splenic; MPV: main portal vein; MB: median branch of splenic; PB: pancreatic branch; SHB: spleen hilar branches.

The cranial mesenteric artery was selected in 66% (43/65) of Wistar rats and was found to be oriented anterocaudally in 91% (39/43) of rats (Fig. 3A). The ileocolic artery was identified in 53% (23/43) of Wistar rats. The right colic artery was identified in 63% (27/43) of Wistar rats while a middle colic artery was not clearly identified (Fig. 3A). In addition, DSA through the cranial mesenteric artery revealed the jejunal branch vessels in 81% (35/43) of Wistar rats numbering from 4–9 visible in each rat (Fig. 3A). The caudal (inferior) mesenteric artery was identified on aortography as described above but was not selected (Fig. 3B).

Figure 3.

Figure 3

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Selective arteriography with catheter tip inserted into cranial mesenteric (A) and at the ostium of caudal mesenteric (B). CrM: cranial mesenteric; RCB: right colic branch; ICCB: ileocecalcolic branch; JA: Jejunal artery; IlA: Iliolumbar; CaM: Caudal Mesenteric Artery; RIA: Right Iliac; LIA: Left Iliac; LCA: left colic.

Variant Anatomy Arteriograms

Numerous anatomic variants were identified on DSA of the abdominal vasculature in Wistar rats. Arteriography revealed the cranial mesenteric artery branching from the celiac trunk in 5% (3/65) of rats (Fig. 4A). Aberrant right hepatic arteries arising from the cranial mesenteric artery were found in 5% (2/43) of rats when selective arteriography of the cranial mesenteric artery was performed (Fig. 4B). In 1 rat, an aberrant left renal artery was found originating from the splenic artery (Fig. 4C). In this case, the left kidney was in an ectopic position and unusual tortuosity of the left renal artery was noted. As described above, while the ostium of the right renal artery was cranial to the left renal artery in most rats, the left renal artery was more cranial in 3 rats (Fig. 4D). Aberrant celiac arteries from the cranial mesenteric artery were found in 7% (3/43) of Wistar rats when selective cranial mesenteric arteriography was performed (Fig. 4E). The branching and distributions of aberrant celiac arteries were normal despite their origins.

Figure 4.

Figure 4

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Selective arteriography demonstrates variant anatomy including an aberrant cranial mesenteric artery arising from the celiac trunk (A), an aberrant right hepatic artery arising from the cranial mesenteric artery (B), an aberrant left renal artery arising from the splenic artery (C), an aberrant ostium of right renal artery (D), and an aberrant celiac artery arising from the cranial mesenteric artery (E). A: aorta; T: tumor; K: kidney; CT: celiac trunk; CrM: cranial mesenteric; SA: splenic; CHA: common hepatic; LGA: left gastric; GDA: gastroduodenal; HPA: hepatic proper; RHA: right hepatic; LRA: left renal; RRA: right renal; LSA: left spermatic artery; CA: celiac.

Magnetic Resonance Imaging and Indirect Angiography of Portal Vein

Given the central role of cross-sectional imaging in informing endovascular arterial interventions, magnetic resonance imaging (MRI) from each rat was analyzed to characterize the lobar and portal venous anatomy. As in humans, the portal vein tributaries accompany the hepatic arteries in their course. The main portal vein and its tributaries were identified on delayed phase DSA 3–5 seconds after contrast injection in the splenic artery in 35 rats (Fig. 5). Several first and second order tributaries of the portal vein were identified on MRI (Supp. Fig. 1). The main course of the portal vein and its tributaries paralleled the intrahepatic arteries (Fig. 2B).

Figure 5.

Figure 5

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Delayed phase common hepatic arteriography demonstrates the main portal vein and its tributaries. MPV: main portal vein; RMPT: right median portal vein tributaries; RLPT: right lateral portal vein tributaries; LMPT: left median portal vein tributaries; LLPT: left lateral portal vein tributaries.

DISCUSSION

These presented data delineate the normal and variant arteriographic anatomy of the rat abdominal vasculature and provide cross sectional imaging correlation to facilitate the application of these rat models for research in endovascular interventions. In so doing, these findings address an important deficiency in the literature.

While the advantages of the rat model for research in endovascular therapies are well known [4, 5, 19–22], there are limited data regarding the vascular anatomy and expected anatomic variation. The growing interest in the study of interventional procedures emphasizes[4, 5, 20] the importance of defining the arteriographic anatomy of the abdominal vasculature to inform these studies. Indeed, these data are expected to facilitate future studies by enabling reductions in contrast, anesthesia, and radiation exposure[23–25]. Furthermore, these findings will aid in experimental design by informing the selection of equipment including catheters and guide wires.

Importantly, these data emphasize the relevance of the rat model for studying a diversity of endovascular interventions. The suitability of this model for interventional oncologic research in liver directed embolotherapy has been described previously and is further underscored by the current study. The celiac artery and associated common hepatic artery branch were selected in each animal of this study. The findings of the current study hold important implications for facilitating these interventions as knowledge of arterial branching patterns are required to limit complications including non-target embolization of organs such as the stomach and pancreas. The anatomy of the celiac axis as well as the branching pattern of the common hepatic artery were clearly defined in each of the 115 rats studied including the relationship of the hepatic arterial branches and the gastroduodenal artery. Interestingly, the ability to select the left gastric artery as well as the renal arteries suggests the opportunity to develop a rat model to study bariatric embolization and targeted interventions for the treatment of vascular anomalies, hemorrhage and neoplasms of the kidney.[20, 26–29]

Similarly, the cranial and caudal mesenteric artery can be readily cannulated with ease. The characterization of these vessels and their branches may facilitate the application of the rat model for studies of interventions for gastrointestinal bleeding or vascular stenosis.[26–29] Indeed, the major branches of the cranial (superior) mesenteric artery and caudal (inferior) mesenteric artery were readily identified including the ileocolic as well as the right and left colic arteries, which provide the major blood supply to the colon.[7–10] The location of the second order cranial and caudal mesenteric branch arteries was variable based on the location of the supplied organs in this cohort of rats. For example, the branching pattern of the jejunal arteries was highly variable and appeared to correlate with the position of the jejunum in a given animal. Similarly, while the colon was often located on the left side of the rat, it may be mobile and its position may then depend on the location of other intra-abdominal organs.

It is important to note that while the rate of successful arteriography was high in this study, these success rates may not be extrapolated given the extensive experience of the operators in performing endovascular interventions in rats[4,5]. While selection of the aorta and first-order branches should be feasible for those with experience in vascular interventions, it is more challenging to select and superselect vascular branches beyond the first-order vessels. In addition, smaller catheters are required to successfully select greater than third order branch vessels.[4,5] In this regard, the utility of this model will be enhanced by further advances in catheter technology including the development of smaller catheters. Nevertheless, this study does confirm that with practice, even these more advanced catheterization techniques can be mastered by interventional radiology investigators.

This study has important limitations. The rats included in this study were part of a parallel project study focusing on liver directed therapy and as a result the data acquired for the abdominal vasculature, other than the celiac axis, must be considered incomplete. The study included only male Wistar and Sprague-Dawley rats and cannot, therefore, account for differences in anatomy based on gender and other rat strains. In addition, hepatocellular carcinoma was induced or inoculated in all rats included in this study. While significant variation in the large vessel anatomy would not be anticipated, differences in the anatomy of distal branch vessels may exist for normal rats. Finally, the arteriograms described in this study primarily included only a ventro-dorsal view. It is possible that superimposition of vessels in this view may have led to the underestimation of the number of hepatic or jejunal arterial branches or the incomplete characterization of the course of other vessels.

In summary, the vascular imaging described in this report provides an overview of normal and variant abdominal arterial anatomy in the rat, a commonly used animal model for vascular interventions. This information can be utilized as a reference during the performance of rat abdominal arterial IR procedures and suggests new applications for this model in IR research.

Supplementary Material

1

Supplemental Figure 1. Magnetic Resonance imaging demonstrates the main portal vein and its tributaries (A–E cross-section view from cranial through caudal, F–I coronal view from posterior through anterior). Delayed phase common hepatic arteriography demonstrates the main portal vein and its tributaries (J). MPV: main portal vein; RPT: right portal vein tributaries; LPT: left portal vein tributaries; RMPT: right median portal vein tributaries; RLPT: right lateral portal vein tributaries; LMPT: left median portal vein tributaries; LLPT: left lateral portal vein tributaries.

Acknowledgments

Financial support: This study was supported in part by the National Institutes of Health, Director’s Office, Grant DP5 OD021391 (TPG).

Footnotes

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Associated Data

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Supplementary Materials

1

Supplemental Figure 1. Magnetic Resonance imaging demonstrates the main portal vein and its tributaries (A–E cross-section view from cranial through caudal, F–I coronal view from posterior through anterior). Delayed phase common hepatic arteriography demonstrates the main portal vein and its tributaries (J). MPV: main portal vein; RPT: right portal vein tributaries; LPT: left portal vein tributaries; RMPT: right median portal vein tributaries; RLPT: right lateral portal vein tributaries; LMPT: left median portal vein tributaries; LLPT: left lateral portal vein tributaries.

NIHMS1531825-supplement-1.pdf (3.5MB, pdf)

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