Neurointervention.  2020 Nov;15(3):107-116. 10.5469/neuroint.2020.00150.

Canine Model for Selective and Superselective Cerebral Intra-Arterial Therapy Testing

Affiliations
  • 1Department of Neurosurgery, Baylor College of Medicine, Houston, TX, USA
  • 2Department of Surgery, Baylor College of Medicine, Houston, TX, USA
  • 3Department of Radiology, Baylor College of Medicine, Houston, TX, USA
  • 4Center for Comparative Medicine, Baylor College of Medicine, Houston, TX, USA

Abstract

Purpose
With advancing endovascular technology and increasing interest in minimally invasive intra-arterial therapies such as stem cell and chemotherapy for cerebral disease, the establishment of a translational model with cerebral circulation accessible to microcatheters is needed. We report our experience catheterizing canine cerebral circulation with microcatheters, present high-resolution angiographic images of the canine vascular anatomy, describe arterial branch flow patterns and provide measurements of canine arterial conduits.
Materials and Methods
Angiograms were performed on 10 intact purpose-bred hounds. Angiography, measurements of arterial conduits and catheterization information for intracranial arterial branches were obtained.
Results
Selective and superselective cerebral angiography was successful in all subjects. Relevant arterial mean diameters include the femoral (4.64 mm), aorta (9.38 mm), external carotid (3.65 mm), internal carotid arteries (1.6 mm), vertebrobasilar system and Circle of Willis branches. Catheterization of the Circle of Willis was achieved via the posterior circulation in all subjects tested (n=3) and the use of flow directed microcatheters resulted in reduced arterial tree deformation and improved superselection of intracranial vessels. Catheterization of the intracranial circulation was attempted but not achieved via the internal carotid artery (n=7) due to its tortuosity and subsequent catheter related vasospasm.
Conclusion
The canine cerebral vasculature is posterior circulation dominant. Anterior circulation angiography is achievable via the internal carotid artery, but direct cerebral arterial access is best achieved via the posterior circulation using flow-directed microcatheters. It is feasible to deliver intra-arterial therapies to selective vascular territories within the canine cerebral circulation, thus making it a viable animal model for testing novel intra-arterial cerebral treatments.

Keyword

Angiography; Animal model; Intraarterial delivery; Neurovascular

Figure

  • Fig. 1. (A) Digital subtraction angiogram via the left common carotid artery (CCA), anteroposterior view. The distal CCA, external (ECA) and internal carotid (ICA) arteries, occipital artery (OA), lingual artery (LA), and maxillary artery (MA) are opacified. Partial filling of the basilar artery (BA) is observed. The severe tortuosity of the left internal carotid artery is also shown. (B) Three-dimensional rotational carotid angiogram, lateral left view highlights the internal carotid artery (ICA) and the severe tortuosity of the carotid artery.

  • Fig. 2. Selective subtracted angiogram of the right internal carotid artery (ICA), anteroposterior view. A microcatheter injection at the ICA highlights the severe tortuosity of the carotid artery. MCA, middle cerebral artery.

  • Fig. 3. Selective digital subtraction angiogram of a microcatheter injection of the basilar artery (BA). The entire Circle of Willis (CoW) is visualized in this anteroposterior view. (A) A flow directed microcatheter injection in the distal the BA shows filling of the superior cerebellar arteries (SCA), posterior cerebral arteries (PCA), posterior communicating arteries (PCoA), middle cerebral arteries (MCA), and anterior cerebral arteries (ACA). Note that the BA maintains its natural curve. (B) A guide catheter injection in the right internal carotid artery (ICA) shows filling of the CoW and highlights the severe tortuosity of the carotid artery.

  • Fig. 4. (A) Digital subtraction angiogram, selective vertebral artery (VA) injection, anteroposterior view. A microcatheter injection at the left VA show fillings of both VA’s, the ventral spinal artery, and the basilar artery (BA) and the Circle of Willis (CoW). (B) Roadmap image of the Echelon 10 microcatheter advanced from the Ramus Spinalis to the Ventral Spinal artery and resultant artery straightening secondary to microcatheter stiffness. (C) microcatheter injection in the proximal left P1 segment demonstrating Echelon 10 microcatheter in the cerebral circulation but with significant straightening of the basilar artery. MCA, middle cerebral artery; ACA, anterior cerebral artery; PCoA, posterior communicating artery; SCA, superior cerebellar artery; PCA, posterior cerebral artery.

  • Fig. 5. (A) Anterior-posterior digital subtraction angiography (DSA) angiogram of the basilar artery and Circle of Willis. The flow directed marathon catheter tip is at the basilar artery bifurcation without deforming the natural basilar artery curvature. (B) Roadmap demonstrating the flowdirected microcatheter being advanced over the wire to the posterior communicating artery) PCoA: carotid junction. (C) Microcatheter contrast injection DSA demonstrating the catheter near the PCoA: carotid artery junction. (D) Pre-catheterization posterior circulation angiogram demonstrating the flowdirected microcatheter in the distal basilar. (E) Road map image showing the flowdirected microcatheter advanced into the right superior cerebellar artery (SCA), making a >180 degree turn without deforming the arterial tree. (F) Superselective contrast injection into the SCA with some reflux into the right PCoA.


Reference

1. Guzman R, Janowski M, Walczak P. Intra-arterial delivery of cell therapies for stroke. Stroke. 2018; 49:1075–1082.
Article
2. Misra V, Lal A, El Khoury R, Chen PR, Savitz SI. Intra-arterial delivery of cell therapies for stroke. Stem Cells Dev. 2012; 21:1007–1015.
Article
3. Moniche F, Escudero I, Zapata-Arriaza E, Usero-Ruiz M, Prieto-León M, de la Torre J, et al. Intra-arterial bone marrow mononuclear cells (BM-MNCs) transplantation in acute ischemic stroke (IBIS trial): protocol of a phase II, randomized, dose-finding, controlled multicenter trial. Int J Stroke. 2015; 10:1149–1152.
Article
4. Silachev DN, Plotnikov EY, Babenko VA, Danilina TI, Zorov LD, Pevzner IB, et al. Intra-arterial administration of multipotent mesenchymal stromal cells promotes functional recovery of the brain after traumatic brain injury. Bull Exp Biol Med. 2015; 159:528–533.
Article
5. Spiliopoulos S, Festas G, Theodosis A, Palialexis K, Reppas L, Konstantos C, et al. Incidence and endovascular treatment of severe spontaneous non-cerebral bleeding: a single-institution experience. Eur Radiol. 2019; 29:3296–3307.
Article
6. Atchaneeyasakul K, Guada L, Ramdas K, Watanabe M, Bhattacharya P, Raval AP, et al. Large animal canine endovascular ischemic stroke models: a review. Brain Res Bull. 2016; 127:134–140.
Article
7. Bouzeghrane F, Naggara O, Kallmes DF, Berenstein A, Raymond J; International Consortium of Neuroendovascular Centres. In vivo experimental intracranial aneurysm models: a systematic review. AJNR Am J Neuroradiol. 2010; 31:418–423.
Article
8. Raymond J, Guilbert F, Metcalfe A, Gévry G, Salazkin I, Robledo O. Role of the endothelial lining in recurrences after coil embolization: prevention of recanalization by endothelial denudation. Stroke. 2004; 35:1471–1475.
9. Shin YS, Niimi Y, Yoshino Y, Song JK, Silane M, Berenstein A. Creation of four experimental aneurysms with different hemodynamics in one dog. AJNR Am J Neuroradiol. 2005; 26:1764–1767.
10. Tilley L, Smith F, Oyama M, Sleeper M. Manual of canine and feline cardiology. 4th ed. St Louis: Saunders;2008.
11. Zhang Y, Jin M, Du B, Lin H, Xu C, Jiang W, et al. A novel canine model of acute vertebral artery occlusion. PLoS One. 2015; 10:e0142251.
Article
12. Mawad ME, Mawad JK, Cartwright J Jr, Gokaslan Z. Long-term histopathologic changes in canine aneurysms embolized with Guglielmi detachable coils. AJNR Am J Neuroradiol. 1995; 16:7–13.
13. Zu QQ, Liu S, Xu XQ, Lu SS, Sun L, Shi HB. An endovascular canine stroke model: middle cerebral artery occlusion with autologous clots followed by ipsilateral internal carotid artery blockade. Lab Invest. 2013; 93:760–767.
Article
14. Lang FF, Conrad C, Gomez-Manzano C, Yung WKA, Sawaya R, Weinberg JS, et al. Phase I study of DNX-2401 (delta-24-RGD) oncolytic adenovirus: replication and immunotherapeutic effects in recurrent malignant glioma. J Clin Oncol. 2018; 36:1419–1427.
Article
15. Srinivasan VM, Chintalapani G, Camstra KM, Effendi ST, Cherian J, Johnson JN, et al. Fast acquisition cone-beam computed tomography: initial experience with a 10 S protocol. J Neurointerv Surg. 2018; 10:916–920.
Article
16. Cloft HJ, Altes TA, Marx WF, Raible RJ, Hudson SB, Helm GA, et al. Endovascular creation of an in vivo bifurcation aneurysm model in rabbits. Radiology. 1999; 213:223–228.
Article
17. Wallace MJ, Ahrar K, Wright KC. Validation of US-guided percutaneous venous access and manual compression for studies in swine. J Vasc Interv Radiol. 2003; 14:481–483.
Article
18. Boulos AS, Deshaies EM, Dalfino JC, Feustel PJ, Popp AJ, Drazin D. Tamoxifen as an effective neuroprotectant in an endovascular canine model of stroke. J Neurosurg. 2011; 114:1117–1126.
Article
19. Lu SS, Liu S, Zu QQ, Xu XQ, Yu J, Wang JW, et al. In vivo MR imaging of intraarterially delivered magnetically labeled mesenchymal stem cells in a canine stroke model. PLoS One. 2013; 8:e54963.
Article
20. Christoforidis GA, Rink C, Kontzialis MS, Mohammad Y, Koch RM, Abduljalil AM, et al. An endovascular canine middle cerebral artery occlusion model for the study of leptomeningeal collateral recruitment. Invest Radiol. 2011; 46:34–40.
Article
21. Rink C, Christoforidis G, Abduljalil A, Kontzialis M, Bergdall V, Roy S, et al. Minimally invasive neuroradiologic model of preclinical transient middle cerebral artery occlusion in canines. Proc Natl Acad Sci U S A. 2008; 105:14100–14105.
Article
22. Ellis JA, Cooke J, Singh-Moon RP, Wang M, Bruce JN, Emala CW, et al. Safety, feasibility, and optimization of intra-arterial mitoxantrone delivery to gliomas. J Neurooncol. 2016; 130:449–454.
Article
23. Peschillo S, Caporlingua A, Diana F, Caporlingua F, Delfini R. New therapeutic strategies regarding endovascular treatment of glioblastoma, the role of the blood-brain barrier and new ways to bypass it. J Neurointerv Surg. 2016; 8:1078–1082.
Article
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