Transauricular Arterial or Venous Access for Cardiovascular Experimental Protocols in Animals Dimitris Karnabatidis, MD, PhD, Konstantinos Katsanos, MD, Athanasios Diamantopoulos, MD, George C. Kagadis, PhD, and Dimitris Siablis, MD, PhD
PURPOSE: To describe a safe percutaneous method of transauricular endovascular access in small and large animals that uses basic catheter-based interventional skills and renders surgery and general anesthesia with intubation unnecessary. MATERIALS AND METHODS: Twenty New Zealand White rabbits and five domestic juvenile swine were used in the experiments. Animals were restrained in the supine position after induction of dissociative anesthesia. Transauricular endovascular access was accomplished by percutaneous catheterization of the auricular artery or vein, roadmap imaging, introduction of a 0.018-inch hydrophilic guide wire, and over-the-wire vascular sheath insertion after serial tract dilations. RESULTS: Technical success rates were 90% and 100% for intraarterial and endovenous access in the rabbit, respectively, and 100% for both routes in the pig. The largest sheaths inserted were 5 F in the rabbits’ aortae, 7 F in the rabbits’ venae cavae, 6 F in the pigs’ aortae, and 8 F in the pigs’ venae cavae. Animal recovery was uneventful, and 48-hour necropsy detected only minor perivascular hematoma in cases of transauricular intraarterial access. Peripheral, intracoronary, intrapulmonary, and intracerebral selective vascular access was safe and feasible. A method of reserving the transauricular endovascular access for future interventions or follow-up by placement of indwelling hydrophilic catheters was also established. CONCLUSIONS: Transauricular endovascular access is a successful technique for establishing and maintaining intraarterial or endovenous vascular access. It obviates surgical cutdown and sacrifice of the femoral and cervical vessels and might considerably improve and expedite cardiovascular experimental protocols in small and large animals. J Vasc Interv Radiol 2006; 17:1803–1811
THE field of experimental cardiovascular intervention comprises various studies of vascular restenosis (1– 4), therapeutic angiogenesis (5–7), embolization treatment (8,9), aneurysm therapy (8,10,11), and research and de-
From the Departments of Radiology (D.K., K.K., A.D., D.S.) and Medical Physics (G.C.K.), School of Medicine, University of Patras, GR 26500, Rion, Greece. Received March 28, 2006; revision requested July 10; final revision received August 16; and accepted August 27. Address correspondence to D.K.; E-mail:
[email protected] None of the authors have identified a conflict of interest. © SIR, 2006 DOI: 10.1097/01.RVI.0000244836.16098.B1
velopment of new interventional techniques and instruments (12,13). Traditionally, intraarterial and endovenous access in an animal is achieved by surgical cutdown of the femoral or cervical arteries and veins, which may be finally ligated and thrombosed, limiting reuse of the vessel (5,10,14,15). These methods are time-consuming, require experienced surgical personnel, and are associated with postsurgical pain and complications such as bleeding, local infections, or systemic sepsis that may turn out to be fatal. A nonsurgical percutaneous technique of endovascular access that could enable rapid, safe, and repeatable cannulation of the central arterial
and/or venous system may serve as an excellent experimental platform for catheter-based diagnostic and therapeutic cardiovascular interventions. The present report demonstrates a minimally invasive method of central vascular access in small and large animals (New Zealand White rabbits and domestic pigs) that uses the auricular artery and vein and obviates surgical sacrifice of the femoral and cervical vessels. A complete series of routine endovascular procedures could be performed through the proposed transauricular endovascular access. Finally, an additional method for reservation of the transauricular access for further or repeated interventions, as well as
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for angiographic or other follow-up of the vessels under study, is described.
MATERIALS AND METHODS The study was conducted according to European Community directives of animal care (16), and the institutional scientific and ethical committee approved the experimental protocols. Twenty New Zealand White rabbits (Oryctolagus cuniculus; weight, 3.0 – 4.0 kg) and five juvenile domestic pigs (Sus scrofa domestica; weight, 20 –25 kg) of either sex were used. Dissociative anesthesia was induced with an intramuscular regimen of atropine (0.04 mg/kg), xylazine (rabbit dosage, 50 mg/kg; pig dosage, 2 mg/kg), and ketamine (rabbit dosage, 50 mg/kg; pig dosage, 10 mg/ kg). Antibiotic prophylaxis with cephalosporin was also administered (750 mg cefuroxime intramuscularly; Zinacef; GlaxoSmithKline, Research Triangle Park, NC). Animals were immobilized in the supine position, and both auricular dorsa (ie, backside surfaces of their ears) were shaved and scrubbed with a combination of povidone iodine and an alcohol-based solution to achieve sterilization. Cardiovascular monitoring was performed with peripheral pulse oximetry. A novice trainee and an experienced interventionalist jointly carried out the transauricular vascular access, selective vessel catheterizations, and diagnostic and therapeutic interventions. All interventional procedures described in this report were performed with standard endovascular instruments. Transauricular Approach A thorough description of the relevant auricular anatomy may be found elsewhere (19,20). Briefly, the central auricular artery, which is a main branch of the external carotid artery, is the feeding ear artery (also called the central ear artery) and follows a straight course along the dorsal surface of the auricle. Venous drainage of the ear is performed by the caudal and rostral auricular veins, which finally merge into the external jugular vein. The diameter of the auricular artery and veins is approximately 1 mm (to a maximum of almost 2 mm in case of the rostral auricular vein) (Fig 1).
Animals were placed under a c-arm unit with ability to perform roadmapping and digital subtraction angiography (Philips DVI-S angiography unit). The central ear artery (10 rabbits) or the marginal ear vein (10 rabbits) was the target vessel for cannulation and endovascular access of the arterial and venous network, respectively. The central auricular artery and vein were cannulated in each of the five pigs. The proposed method included four basic steps. First, the auricular target vessel was punctured with a 22-gauge intravenous catheter (Helmflon; Helm Pharmaceuticals, Hamburg, Germany) approximately at the distal half of its subcutaneous course. The central needle of the catheter was removed, and 5 mL of diluted contrast agent (1:1) was infused to obtain roadmap images of the extracranial carotid or jugular vasculature (14). Second, a 0.018-inch hydrophilic guide wire (V-18 control wire; Boston Scientific, Natick, MA) was carefully advanced into the external carotid artery or external jugular vein. The guide wire was then promoted straight down to the right atrium or left ventricle. Next, the intravenous catheter was withdrawn, local anesthesia (lidocaine 1%) was applied, and a 2- to 3-cm-long incision of the dermis was performed at the point of the initial puncture along the course of the guide wire. Finally, a 4-F, 0.018inch guide wire– compatible vascular sheath (Bolton Medical, Villers-lesNancy, France) was advanced into the external carotid artery or external jugular vein after serial step-by-step dilations with the sheath’s own dilator (Figs 1,2). These repeated over-thewire dilations were necessary to remove the tight and narrow peripheral segment of the artery or vein before sheath insertion. All animals were administered an intravenous bolus of heparin (100 U/kg) after vascular access was established. The time period from initial vessel puncture to successful sheath placement into the appropriate location was recorded in all cases. After transauricular endovascular access was gained, selective catheterization, angiography, angioplasty, and stent implantation of several of the animals’ major arteries and veins was performed with standard instruments. After completion of the interventions, the sheaths were removed, and hemo-
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stasis was achieved with clothespin compression for 10 minutes. Long-term Transauricular Endovascular Access With a view to maintenance of the transauricular endovascular access, we implanted long-term intraarterial or endovenous catheters (three rabbits in each group). After successful transauricular endovascular access and completion of the aforementioned protocol of endovascular techniques, indwelling 4-F hydrophilic catheters (Terumo, Tokyo, Japan) were implanted. The leading end of the catheter was positioned in the superior vena cava or the descending thoracic aorta. The catheters were heparinized (5 mL of 100 IU/mL dilution), the trailing shaft of the catheter was cut, and the catheter’s tail was bent and ligated to assume a hook-like configuration, which was anchored in a small subcutaneous pocket in the rabbit’s ear dorsum to prevent migration. The pocket was closed with a 2-0 running absorbable Vicryl suture (Ethicon, Hamburg, Germany). After a 4-week interval, three-dimensional computed tomography (CT) angiography was performed to assess patency of the cannulated vessels. Subsequently, and under sterile conditions, the ear pocket was incised, and a new vascular access was reattempted with use of a hydrophilic 0.035-inch guide wire (Terumo) through the reserved route under fluoroscopic guidance. Finally, all materials were removed, hemostasis was achieved by compression, and the wounds were left to heal on secondary intention to avoid pocket infection. Follow-up Animals were monitored by expert veterinary personnel during recovery and were closely checked for any signs of local hematomas and local or systemic infection. One group of animals (five rabbits and three pigs with a punctured artery or vein) was killed within 48 hours for necropsy and direct pathologic inspection of the cervical region. Another group of animals (three rabbits with indwelling catheters) was killed for pathologic evaluation after completion of the reattempted transauricular vascular access.
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Figure 1. Endovenous transauricular access in the rabbit. (a) Photograph of a New Zealand White rabbit auricle. Note the gross appearance of the central auricular artery (1), the caudal auricular vein (2), the medial auricular vein (3), and the rostral auricular vein (4). Asterisk denotes the lateral side of the auricle. (b) Direct percutaneous puncture and cannulation of a marginal auricular vein with a 22-gauge intravenous catheter. (c) Roadmap image of the jugular vein (long arrow) and the superior vena cava (short arrow) after vein cannulation. (d) Peripheral tract dilation with the 4-F, 0.018-inch guide wire– compatible vascular sheath after insertion of a 0.018-inch guide wire. (These images appear in color at www.jvir.org.)
Figure 2. Intraarterial transauricular access in the rabbit. (a) Direct percutaneous catheterization of the central auricular artery with a 22-gauge intravenous catheter. Moderate backflow of blood may be observed. (b) Roadmap image of the auricular artery (black arrow) and the common carotid artery (white arrow) after forceful contrast agent infusion through the auricular arterial access. (c) Peripheral tract dilation with the introducer of the 4-F vascular sheath. Repeated tract dilations are required for prompt insertion of the vascular sheath, especially in the case of intraarterial access. (d) Endarterectomy of the distal auricular artery during serial tract dilations. A segment of the endothelium is attached and retrieved on the sheath introducer. (These images appear in color at www.jvir.org.)
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RESULTS Transauricular intraarterial and endovenous access was successful in 90% (nine of 10) and 100% (10 of 10) of the attempted cases in rabbits, respectively. In two cases, puncture of the rabbit central ear artery resulted in severe vasospasm and/or artery transection with subsequent inability to infuse contrast medium and insert the guide wire. In these cases, vascular access was gained through the ear artery of the contralateral auricle. In one case, both auricular arteries were traumatized and the technique was aborted. Consequently, arterial puncture and guide wire insertion were successful in nine of 13 auricular arteries (70% of the ears on an intent-totreat basis). In all animals in which endovenous access was attempted, the method was successful on the first attempt. Mean times to insert the sheath were 8.8 ⫾ 3.2 minutes (range, 5–15 min) and 13.6 ⫾ 5.1 minutes (range, 7–25 min) for jugular and carotid accesses, respectively. After familiarization with the technique in the rabbit platform, simultaneous intraarterial and endovenous access was attempted in the five pigs, with a 100% success rate and a mean procedural period of 16.6 ⫾ 3.2 minutes (range, 13–20 min). The largest sheaths inserted were 5 F in the rabbits’ aortae, 7 F in the rabbits’ venae cavae, 6 F in the pigs’ aortae, and 8 F in the pigs’ venae cavae. Although we tried to place even larger sheaths, the native anatomy of the animals prohibited their accommodation. After transauricular access was achieved, all subsequent catheterization, angiography, and angioplasty/ stent implantation procedures were performed relatively easily with standard interventional instruments. In contrast to the favorable pig heart anatomy, cannulation of the rabbit coronary arteries proved to be technically demanding because of the steep angle of the orifices and the small caliber of the vessels (17). In total, three long-term intraarterial and three endovenous catheters were implanted, with excellent wound healing and no disruption of everyday activity. CT after a 4-week interval revealed that vessel patency of the jugular veins was maintained despite the intraluminal presence of the catheters,
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whereas all three rabbit carotid arteries were occluded (Fig 3). Central vascular access was restored through the reserved route in all endovenous cases and in two of three intraarterial cases. Repeat intraluminal navigation of the guide wire failed in one case of longterm intraarterial access as a result of catheter occlusion and fibrin sheath formation. Animal recovery and viability were normal without any local or systemic complications. No clinical signs of hematoma or neck swelling were identified during follow-up. Necropsy findings included only minor perivascular hematomas after transauricular intraarterial access. No cases of local infection or pocket abscess occurred. Pathologic analysis of the animals with the indwelling catheters showed complete wound healing and scar tissue formation at the points of arterial or venous puncture and a fibrous capsule at the site of the catheters’ pockets.
DISCUSSION The objectives of this study were to demonstrate the safety, feasibility, and potential applications of a nonsurgical, percutaneous technique of transauricular endovascular access in a small and large animal platform. Irrespective of the experimental cardiovascular protocol, arterial or venous catheterizations are traditionally performed after surgical cutdown of the femoral or cervical arteries and veins (5,10,11,14). The peripheral vessels of the rabbit are fragile, and surgical cutdown and catheterization are associated with the need for an experienced surgeon, long procedural time periods, and deep general anesthesia with intubation; dissociative anesthesia usually will not suffice for surgical dissection and handling of the peripheral arteries (5,14). Moreover, the surgically accessed vessel is finally ligated and is usually rendered thrombosed or inaccessible for future access unless a microsurgical suture procedure is performed (5,10,14). Likewise, the pig carotid artery and femoral vessels are vulnerable to iatrogenic trauma and vasospasm and present similar technical difficulties during closed percutaneous or surgical cutdown approaches (18). Although ultrasound guidance or the use of bone
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landmarks have been proposed to assist endovenous vascular access with the Seldinger technique in the pig, surgical cutdown of the pig carotid artery remains the preferred option of carotid cannulation because of its deep location and frequent vasospasm after unsuccessful catheterization attempts (15,18). In the present article, an alternative method for central endovascular access is described that exploits basic catheter skills. The described technique is simple, quick, and straightforward, and it takes advantage of the favorable auricular vascular anatomy of the pig and rabbit, elaborate descriptions of which can be found elsewhere (17–20). The target vessel is cannulated with an intravenous catheter, and then a vascular sheath is inserted according to standard steps of the Seldinger technique (21). Its major advantages are that it accelerates endovascular access, avoids surgical wounds, and, most importantly, completely spares the valuable femoral and cervical vessels. In addition, the subjects experience less pain, bleeding complications, and wound infections. The proposed approach eliminates the need for experienced surgical and anesthesiologic personnel and may be easily performed by a trained interventionalist. Application of dissociative anesthesia sufficed for safe transauricular endovascular access in rabbits and pigs. Apart from its ease and expedience, the technique also has the merits of percutaneous minimally invasive procedures compared with surgery, ie, reduced morbidity and mortality and minimal distortion of normal tissue anatomy and physiology. All complications encountered during the acute establishment of transauricular vascular access were minimal and occurred during the first attempts at transauricular access. As soon as the method was standardized and the operators were familiar with the approach, all procedures were successful and uneventful. In the pig platform, the approach is even more straightforward because of the larger caliber of the pig’s auricular vessels (Fig 4). The most intriguing application of the transauricular endovascular approach is likely the easy and rapid access to the coronary, pulmonary, and cerebral circulation, which may be
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Figure 3. Three-dimensional CT angiography of a rabbit 1 month after implantation of the vascular catheters. Catheters were implanted in the right jugular vein (white arrows) and the left carotid artery (white arrow and circle) in a transauricular manner. Note the course of the left intraarterial catheter behind the mandible and the ipsilateral jugular veins (white arrowhead) (b) compared with the more superficial course of the catheter inside the right jugular vein (anterior view) (c). Unobstructed blood flow around the catheter within the right jugular vein and occlusion of the left carotid artery, probably because of the smaller vessel caliber (anterior views) (a,c). Asterisks denote the trailing ends of the implanted long-term catheters. Note the hook-like configuration of the end of the left intraarterial catheter to help anchoring and prevent migration (posterior view) (b).
particularly useful in more advanced scientific protocols. Because the auricular vessels are branches of the external carotid artery system, straight
access to the ipsilateral cerebral circulation may be also achieved, provided that the vascular sheath is not advanced beyond the origin of the exter-
nal carotid artery. In this way, direct intracoronary or intracerebral drug delivery and interventions in the intracranial and coronary circulation are
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Figure 4. Transauricular intraarterial access in the domestic swine. (a) Introduction of a 5-F vascular sheath at the midpoint of the right common carotid artery (black arrow). (b) Selective catheterization and subtraction angiography of the left renal artery and kidney in the pig. (c) Withdrawal of the sheath at the level of the carotid bifurcation (white arrow) after completion of the procedure. Note visualization of the ascending pharyngeal artery (arrowhead) and the rete mirabile (arrowhead with circle). (d) In addition, bilateral unobstructed cerebral blood flow is depicted.
feasible. However, it should be noted that the domestic swine is unsuitable for intracerebral endovascular procedures because the internal carotid ar-
tery is replaced by the ascending pharyngeal artery and the rete mirabile, which precludes intracranial catheterization (18).
Theoretically, the horizons of the transauricular endovascular approach for the optimization and discovery of novel experimental cardiovascular
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models are endless. Interestingly, the transauricular rabbit model may also serve as a cheap and reproducible platform for realistic in vivo training in catheter-based interventions. The range of training may encompass all aspects of catheterization, angioplasty, and embolization skills for the novice interventionalist. We have also demonstrated that the transauricular route may be exploited for reservation of long-term vascular access with indwelling catheters. Although several reports have addressed the issue of long-term animal vascular access (22– 25), we reported a solely percutaneous approach for repeatable central intraarterial or endovenous access. Although the ear veins may be easily cannulated, extra caution is necessary during puncture of the central ear artery. The regimen of ketamine and xylazine enhances peripheral vasodilation and improves gross visualization of the artery. One should avoid puncturing the artery at its distal quarter or even more peripherally because of its small diameter and should perform a flush with heparinized saline solution to avoid early thrombosis. Initial puncture should aim at the distal half of the vessel, so a second more proximal attempt may be undertaken in case of rupture or vasospasm. Otherwise, the contralateral auricular artery may be accessed. By contrast, venipuncture and endovenous access are significantly easier and quicker. In our experience, the right ear favors endovenous access and the left ear favors intraarterial access so as to provide a relatively straight pathway to the animal’s vena cava and descending aorta, respectively, and avoid excessive sheath bending and vessel kinking during endovascular maneuvers. In case of arterial puncture, mildly forceful infusion of contrast medium was necessary to overcome systolic blood pressure and obtain roadmap images of the common carotid arteries. Although the guide wire is generally easily advanced to the heart under roadmapping, final insertion of the sheath may encounter certain difficulties. In principle, the technique exploits the fact that the auricular vessels are firstorder branches of the external carotid artery and external jugular vein, and it uses a combination of an initial Seldinger technique with serial dilations of the punctured vessel to further
allow insertion of catheters and sheaths that exceed the peripheral caliber of the vessels. Because of the small diameter of the auricular vessels (approximately 1 mm), the cutting of the dermis along the course of the guide wire must be meticulous and extend almost to the base of the ear dorsum. This usually suffices for the endovenous insertion of a vascular sheath because of the distensibility of the venous wall. By contrast, multiple dilations with the sheath dilator are necessary for the step-by-step removal of the small-caliber ear artery and allow for the undisturbed introduction of the sheath into the proximal external carotid artery (Fig 2d). It should be emphasized that, after transauricular endovascular access, the punctured auricular vessel is peripherally destroyed and cannot be accessed again unless a catheter is placed on a long-term basis. Locoregional collateralization compensates for the reduced arterial supply or venous return. In addition, the method necessitates the use of a c-arm unit, resulting in x-ray exposure and increased experiment costs. Finally, through the proposed access, only vascular sheaths of a certain maximum diameter may be inserted (5 F in the rabbit’s aorta, 7 F in the rabbit’s vena cava, 6 F in the pig’s aorta, and 8 F in the pig’s vena cava). This limits the maximum profile of the instruments that may be employed in the experimental protocols. In conclusion, the transauricular approach may serve as a safe, quick, minimally invasive, and highly successful technique to achieve central endovascular access in the rabbit and the pig experimental platforms and obviates surgical cutdown and sacrifice of the peripheral arteries or veins. This method could be easily adopted by the experimental research community and might considerably improve and expedite endovascular experimental protocols in the cardiovascular system. Acknowledgments: The authors gratefully acknowledge the European Social Fund, Operational Program for Educational and Vocational Training II, and the Program PYTHAGORAS II for funding this research.
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