Wang-Zwische Double-Lumen Cannula Leads to Total Cavopulmonary Support in a Failing Fontan Sheep Model

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1 Wang-Zwische Double-Lumen Cannula Leads to Total Cavopulmonary Support in a Failing Fontan Sheep Model Dongfang Wang, MD, PhD, Mark Plunkett, MD, James Lynch, MD, Xiaoqin Zhou, MD, Cherry Ballard-Croft, PhD, and Joseph B. Zwischenberger, MD Department of Surgery, University of Kentucky College of Medicine, Lexington, Kentucky Background. We are developing a total cavopulmonary support system for failing Fontan physiology using the percutaneous Wang-Zwische double-lumen cannula (DLC). Methods. We developed a sheep model of failing Fontan physiology through a right thoracotomy in 5 sheep. An extracardiac conduit was anastomosed to the inferior vena cava and superior vena cava, and a graft was applied to connect the conduit and the right pulmonary artery (PA) to create total vena cava-to-pa diversion, excluding the right heart. The DLC (commercialized as AvalonElite, Avalon Laboratories LLC, Rancho Dominguez, CA) was coupled with a CentriMag pump (Levitronix Waltham, MA) to form a cavopulmonary support system. The DLC was inserted through the right jugular vein and the superior vena cava into the extracardiac conduit with the infusion lumen opening aligned with the right PA bridge. Blood was withdrawn from the superior vena cava and the inferior vena cava through the drainage lumen and pumped into the right PA through the infusion lumen, with flow adjusted to L/min. Results. A successful Fontan model was created without cardiopulmonary bypass. After total venous blood diversion from the vena cava to the right PA artery, failing Fontan physiology developed, evidenced by elevated central venous pressure and dropping mean PA pressure and systolic arterial pressure. The DLC was successfully inserted, and hemodynamics were normalized in all 5 sheep for the duration of the 2-hour study. Conclusions. We created a model of failing Fontan circulation in sheep without cardiopulmonary bypass. The DLC system achieved total cavopulmonary support for 2 hours in our failing Fontan sheep model. (Ann Thorac Surg 2011;91: ) 2011 by The Society of Thoracic Surgeons Fontan circulation lacks a right ventricle (RV) to pump blood to the lungs and requires a higher than normal central venous pressure (CVP) to drive venous blood through the pulmonary circulation. Any increase of pulmonary circulatory resistance will further elevate CVP to initiate failing Fontan circulation, which is associated with a perioperative mortality rate of 20% as well as a high rate of late morbidity and mortality [1]. A persistently elevated CVP results in peripheral tissue fluid retention, protein-losing enteropathy, pleural effusion, ascites, hepatic congestion, and compromises the function of the major systemic organs (eg, liver, kidney, heart). Elevated pulmonary vascular resistance and reduced pulmonary blood flow results in inadequate lung perfusion, poor oxygenation, reduced preload of the single ventricle, reduced cardiac output, and poor systemic perfusion. Failing Fontan physiology often results in removal from the heart transplant waiting list or a higher morbidity and mortality rate after heart transplant. [2] A technique to provide support of the failing Fontan circulation may have a significant effect on early survival and serve as a bridge to transplant in the event of persistent failure. A cavopulmonary (CP) assist device (CPAD) would allow for active pumping from the inferior vena cava (IVC)/superior vena cava (SVC) to the pulmonary artery (PA), resulting in a decreased CVP and an increase in pulmonary blood flow. Lowering the CVP will also promote improved lymphatic drainage and lessen venous congestion, thereby improving protein-losing enteropathy, ascites, and congestion of the liver and other organs. Higher pulmonary blood flow will improve pulmonary perfusion and enhance gas exchange. This will also augment the ventricular preload, resulting in improvements in cardiac output and major organ perfusion. Accepted for publication Feb 11, Presented at the Basic Science Forum of the Fifty-seventh Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 3 6, Address correspondence to Dr Zwischenberger, Department of Surgery, University of Kentucky College of Medicine, 800 Rose St, MN264, Lexington, KY ; jzwis2@uky.edu. Dr Zwischenberger discloses that he has financial relationships with Avalon, MC3, Ikaria, and Novalung; Dr Plunkett with Thoratec Corp; and Dr Wang with Avalon by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur

2 Ann Thorac Surg WANG ET AL 2011;91: DLC LEADS TO TOTAL CAVOPULMONARY SUPPORT 1957 Abbreviations and Acronyms CP cavopulmonary CPAD cavopulmonary assist device CVP central venous pressure DLC double-lumen catheter HR heart rate IVC inferior vena cava LA left atrium LPA left pulmonary artery LV left ventricle mpap mean pulmonary artery pressure PA pulmonary artery RA right atrium RPA right pulmonary artery RV right ventricle SABP systolic arterial blood pressure SVC superior vena cava VV-ECMO venovenous extracorporeal membrane oxygenation Our previous successful development of a double lumen cannula (DLC) for venovenous extracorporeal membrane oxygenation (VV-ECMO) showed that a single DLC allowed the blood to be withdrawn from both the SVC and IVC through one lumen and infused to the RA through another lumen [3 5]. We therefore hypothesized that this DLC could also fit the Fontan anatomy to withdraw blood from the SVC and IVC to deliver blood directly to the PA through Fontan anastomoses. By coupling this DLC with any commercially available blood pump, it should achieve almost total CP support without a major operation. In this study, we tested our hypothesis on a sheep model of falling Fontan circulation. Material and Methods The DLC-Based CPAD Our percutaneous CPAD consists of our patented DLC (AvalonElite, Avalon Laboratories LLC, Rancho Dominguez, CA) and a compact CentriMag pump (Levitronix Waltham, MA). The DLC is the critical component and is inserted from the jugular vein into the SVC and extracardiac conduit. The infusion opening is aligned with the right PA (RPA), the proximal drainage openings are positioned in SVC above the Fontan anastomosis for upper body venous drainage, and the distal end drainage openings are positioned below for lower body drainage (Fig. 1A). When connected to the CentriMag pump, the DLC will withdraw venous blood from the SVC/IVC and pump it back into the RPA through the bridge graft, accomplishing CP support. Animal Preparation and Instrumentation All animal studies were approved by the University of Kentucky Institutional Animal Care and Use Committee and were conducted in accordance with the Principles of Laboratory Animal Care (National Society of Medical Research) and the Guide for the Care and Use of Laboratory Animals (National Institutes of Health publication 85-23, revised 1996). The CPAD was tested in our sheep model of failing Fontan physiology. The study used 5 adult female crossbred sheep (weight, kg). After anesthesia induction Fig 1. (A) The cavopulmonary assist device consists of a Wang- Zwiche double-lumen catheter (DLC; AvalonElite, Avalon Laboratories LLC, Rancho Dominguez, CA) and a CentriMag Pump (Levitronix Waltham, MA). The DLC removes venous blood from superior vena cava (SVC)/inferior vena cava (IVC) and delivers it to the right pulmonary artery (RPA). (B) In the sheep model of failing Fontan circulation, the extracardiac conduit diverts total venous blood from SVC/IVC to RPA. (LA left atrium; LPA left pulmonary artery; LV left ventricle; RA right atrium; RV right ventricle.)

3 1958 WANG ET AL Ann Thorac Surg DLC LEADS TO TOTAL CAVOPULMONARY SUPPORT 2011;91: with intravenous ketamine (5 mg/kg) and diazepam (0.25 mg/kg), the sheep were intubated with an endotracheal tube (Hudson RCI, Triangle Research Park, NC), transferred to the operating room, and connected to the anesthesia machine (Narkomed 2B North American DRAGER, Telford, PA). Prophylactic analgesia with buprenorphine (0.005 to 0.010mg/kg) was administered intramuscularly. Anesthesia was maintained by 1% to 3% isoflurane (Butler Animal Health Supply, Dublin, OH), with titration for a normal range of heart rate and arterial blood pressure. Femoral arterial and venous catheters (BD Intracath, Becton Dickinson Infusion Therapy Systems Inc, Sandy, UT) were placed by a cutdown in the right groin. Creation of Failing Fontan Sheep Model A right lateral thoracotomy was performed through the fourth intercostal space. The main PA was identified and exposed. A purse string was placed on the root of the main PA and a 16F arterial catheter was placed into the PA through the purse string for PA pressure monitoring. The right atrium, SVC, and IVC were identified and exposed. The long IVC in sheep (as long as 10 cm) allows side-biter clamping for the anastomosis without interruption of IVC blood flow, therefore eliminating the requirement for cardiopulmonary bypass. The azygos vein was tied and cut to isolate the SVC. A 10-cm extracardiac conduit (18- mm OD Gore-Tex graft, W. L. Gore and Associates, Flagstaff, AZ) was anastomosed between the SVC and IVC in end-to-side fashion. The transverse pericardial sinus was accessed from the right side of the SVC to expose the entire RPA (Fig 1B). A side-biter clamp was applied on the RPA, and a 2.0-cm incision was made in a longitudinal direction for a bridge graft anastomosis. A 3-cm bridge graft (18-mm OD Gore- Tex) was anastomosed to the RPA and an extracardiac conduit in end-to-side fashion to create a connection between the SVC/IVC and the pulmonary circulation. As 2 clamps were placed on the SVC and IVC between the atrium and the SVC/IVC anastomoses, the total venous blood was diverted from the SVC/IVC to PA circulation through the extracardiac conduit and bridge graft. The 2.0-cm anastomoses between the RPA and the bridge graft limited the blood flow from the extracardiac conduit into the RPA, resulting in a failing Fontan circulation. CP Support for Failing Fontan Circulation in Sheep Model After the failing Fontan circulation was established, the DLC was deployed for CP support. The right jugular vein was exposed through a 2-cm cutdown. After a bolus intravenous injection of heparin (100 U/kg), the DLC was inserted from the right jugular vein into the SVCextracardiac conduit. The CentriMag pump was connected to the DLC and pumped blood at a flow rate of 1 to 2 L/min. The DLC was adjusted to align the infusion opening with the bridge graft anastomosis and the RPA. Two DLC drainage lumen openings were located in the extracardiac conduit. The proximal drainage side openings were above the bridge graft to withdraw venous blood from the SVC, and the distal drainage end openings were below the bridge graft to withdraw venous blood from the IVC. Therefore, venous blood from both the SVC and the IVC was pumped back into pulmonary circulation through the DLC infusion lumen, which was opened toward the bridge graft and the RPA. The CentriMag pump was adjusted to increase the pump flow rate to L/min until total CP support was achieved, as evidenced by the CVP being lower than mean pulmonary artery pressure (mpap). Data Collection and Analysis The femoral arterial/venous catheters and PA catheter were connected to transducers (Edwards Lifesciences, Irvine, CA) for pressure monitoring. Arterial blood pressure, CVP, and mpap were continuously monitored during the operation by a Phillips MP-50 monitor (Boeblingen, Germany). Systolic arterial blood pressure, mpap, and CVP were recorded to differentiate a change among the status of control (normal baseline), failing Fontan circulation, and CP support. The DLC was carefully positioned for proper alignment and best CP support at every data point. All data are expressed as mean standard deviation. A value of p 0.05 was considered statistically significant. Differences between the intervals were evaluated using the Student t test. Results A successful failing Fontan model was created in the 5 sheep without cardiopulmonary bypass support (Fig 1B). After clamps were placed on the SVC and IVC between the right atrium and anastomosis, total venous blood was diverted from the SVC/IVC to the RPA through the extracardiac conduit into the pulmonary system, bypassing the right atrium and RV. Because there is no RV in the pulmonary circulation, an elevated CVP cannot overcome the high resistance from the long conduit and the limited size of the anastomoses, thus creating a failing Fontan circulation. Compared with the control, the failing Fontan circulation was characterized by a low mpap, high CVP, and systemic hypotension (Table 1). The mpap was significantly decreased, from to (p 0.01). The CVP increased from to mm Hg (p 0.01). The systolic arterial blood pressure dropped from to mm Hg (p 0.01). The heart rate remained unchanged. After DLC implantation, CP support was established at a pump flow rate of L/min. As the CPAD pumped blood from the vena cava into the pulmonary circulation, functioning as a right heart, the failing Fontan circulation was immediately corrected, with hemodynamics reversed to the level of normal baseline (Table 1). Compared with the failing Fontan status, the systolic arterial blood pressure was increased to mm Hg, mpap increased to mm Hg, and CVP dropped to mm Hg at 30 minutes of CP support.

4 Ann Thorac Surg WANG ET AL 2011;91: DLC LEADS TO TOTAL CAVOPULMONARY SUPPORT 1959 Table 1. Hemodynamic Variables a Cavopulmonary Support Variable Normal Baseline Failing Fontan 30 min 60 min 90 min 120 min HR. beats/min SABP, mm Hg b mpap, mm Hg b CVP, mm Hg b a Cavopulmonary support completely reversed the abnormal hemodynamics of failing Fontan circulation. b Indicates p 0.01 vs normal baseline. CVP central venous pressure; HR heart rate; mpap mean pulmonary artery pressure; SABP systolic arterial blood pressure. These hemodynamic indicators remained stable at physiologic baseline levels throughout the 2-hour experimental CP support, with no need for inotropic support (Table 1, Fig 2). The CPAD pumped blood against the pressure gradient from the lower-pressure SVC/IVC to the higherpressure RPA, indicating total CP support. Comment The Fontan procedure is lifesaving for many patients but confers high morbidity and mortality both short-term and long-term because of failing Fontan circulation. Venoarterial ECMO is currently the best option to assist the patient with failing Fontan circulation [6 8]. However, ECMO has a time limit, is labor intensive, expensive, and traumatic to the blood. The bulky ECMO system includes an oxygenator, complex circuit, and full anticoagulation. ECMO is also nonambulatory and is associated with a high morbidity and mortality rate [9]. A B C Fig 2. Hemodynamic stability of cavopulmonary support. (A) Normal baseline. (B) Failing Fontan circulation. The systolic arterial blood pressure and mean pulmonary artery pressure (mpap) were reduced, and central venous pressure (CVP) was elevated after total cavopulmonary conversion. (C) The abnormal failing Fontan hemodynamic variables were completely corrected by cavopulmonary support. A double Hemopump (Medtronic, Inc, Minneapolis, MN) was tested on sheep to support the failing Fontan by pumping blood into the PA from the IVC/SVC [10]. Unfortunately, the procedure was complicated and traumatic, and the Hemopump is no longer commercially available. Several catheter-based pumps are designed for CP support [11 14]. They all use integrated blades driven by a long mechanical shaft. The fast moving blades require cage protection, complicating catheter pump insertion, deployment, and alignment. Their design is innovative but presents engineering challenges. At the present time, there is also no working prototype for in vivo testing to prove CP support. Anatomic Characteristics of the Fontan Circulation and Challenge of CPAD Installation In the Fontan procedure, the SVC and IVC individually are directly connected to the RPA. There is no reservoir for the drainage cannula to collect the venous blood, and the PA is not ideal for infusion because the blood delivered can flow back to the IVC/SVC through the Fontan connection. This configuration makes the connection of a right ventricular assist device (RVAD) to the Fontan circulation challenging. Currently, to use an RVAD for CP support, the Fontan connection must be taken down while the patient is on cardiopulmonary bypass [15]. The DLC Fits Fontan Anatomy for CP Support In VV-ECMO, three venous cannulations are required to avoid blood recirculation for total gas exchange performance [16]. We (D.W. and J.B.Z.) have designed a patented DLC for efficient VV-ECMO [17]. In our DLC, one drainage lumen withdraws total venous blood from SVC and IVC, and the infusion lumen leads blood toward the tricuspid valve. One DLC venous cannulation can achieve up to total gas exchange performance with negligible recirculation. This single-site DLC venous cannulation with a simple, short circuit can achieve the same function as the previous triple-venous cannulations with a complicated, long circuit for VV-ECMO [3 5, 16]. Because the SVC and IVC are directly connected to the RPA, this DLC also fits into the Fontan anatomy for CP support. Inserted through the right jugular vein, our DLC splits drainage sites, one in the SVC and the other in the IVC, and allows for drainage of total venous blood

5 1960 WANG ET AL Ann Thorac Surg DLC LEADS TO TOTAL CAVOPULMONARY SUPPORT 2011;91: through one drainage lumen while the infusion lumen in the same DLC infuses blood to the RPA. Coupling with a commercial blood pump, our DLC can move total venous blood from the vena cava to the PA, providing total CP support and augmenting pulmonary circulation. In our current study, the DLC was easily inserted into the right jugular vein and deployed in the CP anastomoses. This DLC-based CPAD immediately reversed the failing Fontan circulation, normalizing high CVP, low mpap, and low systolic pressure. Through the 27F DLC, venous blood was continuously pumped from the vena cava to the RPA against the mpap-cvp pressure gradient to maintain higher mpap and lower CVP, demonstrating total CP support. The DLC-based CPAD has no moving parts inside the patient s body, eliminating the related mechanical complications. In clinical practice, current DLC-based VV- ECMO showed an adult patient s right IVC is large enough to accommodate a 31F DLC, which can handle blood flow of up to 5.5 L/min [5]. This amount of flow will allow total CP support for most patients. In the current study, proper positioning of the DLC was critical for best performance. About Our Animal Model We developed a very simple sheep model to mimic failing Fontan circulation and demonstrated the proof of concept of DLC-based CP support. The long IVC above the diaphragm in sheep allows side (IVC) to end (conduit) anastomosis without interfering with blood flow, eliminating the requirement of cardiopulmonary bypass. Our current animal model mimics Fontan physiology but does not exactly match human Fontan anatomy. For the future preclinical testing of the new DLC-based CPAD, a sheep model mimicking human Fontan anatomy will be required. The Limitation The current DLC is not designed for CP support application. The blood flow comes out of the infusion lumen in one direction, which only perfuses one lung instead of both lungs. Furthermore, like all the other catheter-based CPADs, our DLC also requires precise alignment of the infusion lumen opening to the PA for efficient blood delivery and for best CP support performance. A new DLC design is required to achieve bidirectional perfusion and dependable alignment. In conclusion, our current preliminary in vivo sheep study showed a practical DLC-based CPAD with easy insertion, advancement, and deployment, and great CP support performance. However, the current commercial DLC is not designed to support the patient with failing Fontan circulation. A specific DLC design is required to better fit human Fontan anatomy for better performance and infusion alignment. References 1. Khairy P, Fernandes SM, Mayer JE Jr, et al. Long-term survival, modes of death, and predictors of mortality in patients with Fontan surgery. Circulation 2008;117: Bernstein D, Naftel D, Chin C, et al. Outcome of listing for cardiac transplantation for failed Fontan: a multiinstitutional study. Circulation 2006;114: Wang D, Zhou X, Liu S, Sidor B, Lynch J, Zwischenberger JB. Wang-Zwische double lumen cannula-toward a percutaneous and ambulatory paracorporeal artificial lung. ASAIO J 2008; 54: Kiernan MS, Krishnamurthy B, Kapur NK. Percutaneous right ventricular assist via the internal jugular vein inc ardiogenic shock complicating an acute inferior myocardial infarction. J invasive Cardiol 2010;22:E Bermudez CA, Rocha RV, Sappington PL, Toyoda Y, Murray HN, Boujoukos AJ, Initial experience with single cannulation for venovenous extracorporeal oxygenation in adults. Ann Thorac Surg 2010;90: Rogers AJ, Trento A, Siewers RD, et al. Extracorporeal membrane oxygenation for postcardiotomy cardiogenic shock in children. Ann Thorac Surg 1989;47: Salvin JW, Scheurer MA, Laussen PC, et al. Factors associated with prolonged recovery after the fontan operation. Circulation 118:2008;118:S Booth KL, Roth SJ, Thiagarajan RR, ALmodovar MC, del Nido PJ, Laussen PC. Extracorporeal membrane oxygenation support of the Fontan and biodirectional Glenn circulations. Ann Thorac Surg 2004;77: Chaudhari M, Sturman JU, O Sullivan J, et al. Rescue cardiac transplantation for early failure of the Fontan-type circulation in children. J Thorac Cardiovasc Surg 2005;129: Rodefeld MD, Boyd JH, Myers CD, et al. Cavopulmonary assist: circulatory support for the univentricular Fontan circulation. Ann Thorac Surg 2003;76:1911 6; discussion Throckmorton AL, Ballman KK, Myers CD, Frankel SH, Brown JW, Rodefeld MD. Performance of a 3-bladed propeller pump to provide cavopulmonary assist in the failing Fontan circulation. Ann Thorac Surg 2008;86: Throckmorton AL, Kapadia J, Madduri D. Mechanical axial flow blood pump to support cavopulmonary circulation. Int J Artif Organs 2009;31: Kapadia JY, Pierce KC, Poupore AK, Throckmorton AL. Hydraulic testing of intravascular axial flow blood pump designs with a protective cage of filaments for mechanical cavopulmonary assist. ASAIO J 2010;56: Rodefeld MD, Coats B, Fisher T, et al. Cavopulmonary assist for the univentricular Fontan circulation: von Karman viscous impeller pump. J Thorac Cardiovasc Surg 2010;140: Pretre R, Haussler A, Bettex D, Genoni M. Right-sided univentricular cardiac assistance in a failing Fontan circulation. Ann THorac Surg 2008;86: Ichiba S, Peek GJ, Sosnowski AW, Brennan KJ. Firmin RK. Modifying a venovenous extracorporeal membrane oxygenation circuit to reduce recirculation. Ann Thorac Surg 2000; 69: Wang D, Zwischenberger JB. Single expandable double lumen cannula assembly for veno-venous ECMO. In: United States Patent and Trademark Office (ed. USPTO); The University of Texas System USA, 2009.

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