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W tym Artykule

  • Podsumowanie
  • Streszczenie
  • Wprowadzenie
  • Protokół
  • Wyniki
  • Dyskusje
  • Ujawnienia
  • Podziękowania
  • Materiały
  • Odniesienia
  • Przedruki i uprawnienia

Podsumowanie

This protocol describes the surgical methodology for implanting a large animal wireless telemetry device to enable continuous and long-term collection of hemodynamic data, including heart rate, arterial blood pressure, inferior and superior vena cava pressures, and cardiac rhythm.

Streszczenie

While the Fontan procedure drastically improves life expectancy for patients with single ventricle, it is well recognized that the resulting circulation causes significant disease burden long term as a consequence of chronically elevated central venous pressures and decreased cardiac output. Chronic Fontan animal models are a valuable asset to studying the late physiological outcomes associated with this operation and a necessary tool in the evaluation of future devices designed to alleviate Fontan failure. However, previous attempts at the creation of chronic Fontan models have been hindered by poor survival rates. Additionally, effective hemodynamic data collection poses a significant challenge in freely moving animals. To this end, the use of wireless implantable telemetry systems provides a novel solution for real-time and long-term monitoring of cardiovascular data. This protocol describes the methodology for surgical implantation of a wireless telemetry device in a Fontan survival ovine model, facilitating the continuous and ongoing recording of several hemodynamic parameters, including heart rate, arterial blood pressure, and localized pressures in the inferior (IVC) and superior vena cava (SVC). Telemetry devices were implanted with cannulation of either the carotid artery and internal jugular vein or femoral artery and vein, for placement of pressure-sensing catheters in the ascending aorta and SVC or abdominal aorta and IVC, respectively. The use of the wireless telemetry systems enabled close postoperative monitoring following a single-stage Fontan operation, which contributed to improved animal welfare and survival.

Wprowadzenie

The development of the Fontan procedure in 1971 led to significant improvements in outcomes for patients with single ventricle1. The purpose of this operation is to separate systemic and pulmonary venous return to the heart, thereby increasing systemic oxygenation and relieving volume load on the systemic ventricle. Since its introduction, numerous modifications have been made to the surgical approach. Currently, total bypass of the right heart is most often achieved through staged reconstruction2,3. Typically, the first stage is performed during the first week of life4. Patients then undergo a second stage, which consists of either the Glenn procedure or hemi-Fontan, to redirect blood flow from the superior vena cava (SVC) to the pulmonary artery (PA)5. This is followed by the Fontan procedure, which involves the creation of an extracardiac conduit or lateral tunnel between the inferior vena cava (IVC) and PA6. Surgical advancements such as those made throughout the history of the Fontan procedure could not have been achieved without the use of animal models7.

While the Fontan procedure drastically improves life expectancy for single ventricle patients, it is well recognized that the resulting circulation, which operates without a subpulmonic pump, causes significant disease burden in the long term as a consequence of chronically elevated central venous pressures (CVP) and decreased cardiac output8,9,10,11,12. Chronic Fontan animal models are a valuable asset to studying the late physiological outcomes associated with this operation13. Active data collection of cardiovascular parameters, such as CVP, heart rate, and other vital signs, to capture the postoperative hemodynamic changes is essential for a comprehensive evaluation of developing pathophysiology. Furthermore, animal models are a necessary tool for testing the capability of novel ventricular assist devices designed to alleviate the hemodynamic shortcomings of the Fontan circulation in vivo14,15,16,17,18,19.

However, effective data collection poses a significant challenge. Invasive catheter-based techniques are limited by their transient nature, associated procedural risks, and the inability to monitor the animal's condition over extended periods. Moreover, previous attempts to create a large animal Fontan model have been hindered by poor survival rates, presumably due to the failure of normal hearts to adapt to the acute establishment of the Fontan circulation7,20. To this end, the use of wireless telemetry systems provides a novel solution for real-time, long-term collection of cardiovascular data in freely moving animals21,22. These devices may also enable close postoperative monitoring, which could lead to improved animal welfare and survival.

Here, we describe the methodology for the successful implantation and use of a wireless telemetry system23 in a chronic Fontan ovine model. This technique provided a robust and reliable means of continuous hemodynamic data collection, enabling the study of venous pressures and other key physiological parameters. Implementation of this technology in preclinical models is critical for advancing our understanding of Fontan physiology and the development of new therapeutic strategies aimed at improving the long-term outcomes of Fontan patients.

Protokół

This experimental protocol was approved by the Institutional Animal Care and Use Committee of the Nationwide Children's Hospital Abigail Wexner Research Institute (AR20-00121). All procedures adhered to the guidelines outlined in the National Institute of Health's Guide for the Use and Care of Laboratory Animals. This research followed the Animal Research: Reporting of In Vivo Experiments guidelines. Dorset sheep with a weight range of 23-38 kg and an age range of 2-12 months were housed in a specific pathogen-free environment with free access to food and water for at least 1 week before surgery. The equipment and reagents used in the study are listed in the Table of Materials.

1. Animal preparation

  1. Have the sheep undergo evaluation by the veterinary team 1 week prior to surgery to ensure that they can safely undergo anesthesia. Fast healthy sheep and deprive of water for 12 h prior to the surgical procedure.
  2. Sedate with a combination of ketamine (4 mg/kg) and diazepam (0.5 mg/kg) injected through an internal jugular (IJ) vein.
  3. Shave sheep according to the planned procedure (detailed below) and over the thigh for electrocautery grounding pad placement. Clean the surgical sites with alcohol.
  4. Insert an 8-9 mm single-lumen endotracheal tube into the trachea.
  5. Insert an orogastric tube for decompression of the stomach and rumen.
  6. Insert a single-lumen venous catheter (16-18 G) into the right jugular vein or a lateral saphenous vein for continuous fluid administration, continuous rate infusion (CRI) of propofol, and drug injection as needed.
  7. Place an arterial line (22-24 G) in an auricular artery for continuous blood pressure monitoring.
  8. Place a blood pressure cuff on the right front limb for non-invasive blood pressure measurement, a clip on the ear or tongue to monitor oxygen saturation, and electrocardiogram (ECG) leads on all four limbs.
  9. During the procedure, maintain anesthesia using inhaled isoflurane 1%-3% with 100% O2 and/or propofol CRI (20-45 mg/kg/h).
  10. Aseptically clean the surgical sites using a chlorhexidine-based prep and drape in the standard sterile fashion.
  11. Administer cefazolin (25 mg/kg) for antibiotic prophylaxis before incision and re-dose every 4 h during the operation as needed.
  12. Administer a subcutaneous injection of local anesthetic, such as bupivacaine 0.25%, at all planned incision sites prior to incision.

2. Telemetry device preparation

  1. Open the telemetry software program and turn on the telemetry device using the magnet switch while it is still sealed in its original packaging.
  2. Within the software program, click on Hardware located at the top bar and select Edit PhysioTel Digital (CLC) Configuration to assign the telemetry unit to a communication link controller (CLC).
  3. Once a CLC is selected, its CLC Details page will open. Within this page, click on Search for Implants, which will initiate a search for implant devices that are turned on nearby.
  4. Click Add to add the telemetry unit to the Implants Selected list. The device will now appear under the Configured Implants list on the CLC Details page. Click Save and Exit.
  5. Start data acquisition by pressing the Play button next to the name of the telemetry unit in the Sampling Control tab. Graph displaying the live data acquisition will automatically open.
  6. Remove the device from its exterior packaging and transfer it to its sterile interior packaging onto the operating table.
  7. Zero the device while it remains in its interior packaging. Wait until measurements from the device have been stable for 30 s and use the stabilized non-pulsatile mean (NPMN) pressure values as the offset.
  8. Within Subject Setup, select the settings icon next to the parameter that is being zeroed and open the Offsets tab. Enter the offset value obtained from the NPMN measurements into the text box.
  9. After inputting the offset, check if the NPMN readings are 0 ± 0.1 mmHg. If not, repeat step 2.7 until values are within the desired range.
  10. Perform steps 2.7-2.9 for both pressure channels.
  11. Before inserting the pressure-sensing catheters into a blood vessel, tap the tip to identify its corresponding channel. Taps will become apparent in the waveform output.
  12. Use the catheter corresponding to the left ventricular pressure (LVP) channel for arterial pressure measurement and the blood pressure (BP) channel for venous pressure measurement.
  13. Within the Standard Attributes tab of the Blood Pressure Analysis Attributes dialog box, set the minimum pulse height to 1 mmHg for the BP channel.

3. Method 1: Femoral artery and vein cannulation

  1. Shave the sheep in a wide perimeter around the right groin and over the abdomen and chest.
  2. Position the sheep supine on the operating table with their front limbs secured in flexion using a flexible cloth belt and hind limbs secured in extension using a slipknot tie to allow for access to the groin (Figure 1A).
  3. Make a 5-cm transverse incision in the right inguinal region centered over the palpable femoral artery, approximately 1 cm below the inguinal crease.
  4. Using a combination of electrocautery and blunt dissection, dissect through the subcutaneous tissue to the femoral triangle. Locate the femoral vessels by palpating for the arterial pulse.
  5. Divide between the sartorius and adductor longus muscle along the direction of the muscle fibers to expose the femoral vessels (Figure 1B).
  6. Using a combination of blunt and sharp dissection, clear the connective tissue from the femoral vessels circumferentially.
  7. Pass a double-looped 2-0 silk tie around both vessels proximal and distal to the cannulation site for temporary vessel ligation.
  8. Make a 6-cm transverse incision through the skin in the right lower abdomen, approximately 3 cm above the inguinal crease.
  9. Using a combination of electrocautery and blunt dissection, dissect through the subcutaneous fat and connective tissue to create a 6 cm x 4 cm pocket superficial to the external oblique.
  10. Insert the telemetry device into the subcutaneous pocket and secure it in place using a 2-0 silk suture (Figure 1C).
  11. Tunnel the telemetry device antenna under the subcutaneous tissue and secure it in place using a 2-0 silk suture.
  12. For placement of the biopotential (ECG) leads, make 1-cm counter incisions in the skin over the mid and lower abdomen, as well as the lower and upper chest. Tunnel subcutaneously to connect these incisions to the device body pocket and guide the ECG leads to their desired location.
  13. Place the positive electrode in the subcutaneous tissue to the left of the lower sternum. Ensure that the silicone tubing is removed to reveal the tip of the steel wire underneath.
  14. Place the negative electrode in the subcutaneous tissue to the right of the upper sternum.
  15. Excess wiring for both leads can be coiled and secured in the subcutaneous location using a 2-0 silk suture.
  16. Create a subcutaneous tunnel from the lower abdominal device pocket to the inguinal incision and thread the two pressure catheters through.
  17. Place a purse-string stitch using a 6-0 polypropylene suture around the cannulation site of both the femoral artery and vein, which can be secured using a plastic tourniquet.
  18. Fill the catheter gel tips with non-compressible, high-viscosity gel to prevent coagulation inside the catheter tips, ensuring no air bubbles.
  19. Administer a dose of intravenous heparin (100 units/kg) 3 min before cannulation.
  20. Tighten the proximal and distal 2-0 silk tourniquets around the femoral artery. Carefully incise into the vessel at the center of the purse-string stitch using a #11 blade scalpel and dilate slightly with the tip of a curved hemostat.
  21. Insert the pressure catheter corresponding to the LVP channel and advance it into the abdominal aorta, loosening the proximal silk tourniquet to allow for passage of the catheter. Tighten the purse-string suture and tie it around the catheter.
  22. Repeat steps 3.20 and 3.21 for femoral vein cannulation using the pressure catheter corresponding to the BP channel and advance it into the abdominal IVC (Figure 1D).
  23. Confirm that the catheter tips are located appropriately in the IVC and aorta using fluoroscopy.
  24. Reapproximate the sartorius muscle using a 2-0 absorbable suture.
  25. Close the skin with deep dermal and subcuticular sutures using 3-0 and 4-0 absorbable sutures, respectively.

4. Method 2: Carotid artery and internal jugular vein cannulation

  1. Shave the sheep in a wide perimeter around the left neck and down over the chest.
  2. Position the sheep in right lateral decubitus on the operating table with the left front limb secured in flexion using a slipknot tie to expose the chest (Figure 2A).
  3. Make a 5-cm longitudinal skin incision above the left carotid artery and IJ vein, approximately 7 cm cranial to the thoracic inlet.
  4. Using electrocautery, dissect through the subcutaneous fat, connective tissue, and platysma to expose the neck vessels (Figure 2B).
  5. Using a combination of blunt and sharp dissection, clear the connective tissue from the left carotid artery and IJ vein circumferentially.
  6. Pass a double-looped 2-0 silk tie around both vessels proximal and distal to the cannulation site for temporary vessel ligation.
  7. Make a 6-cm longitudinal incision at the base of the left neck between the scapula and cervical spine.
  8. Using a combination of electrocautery and blunt dissection, dissect through the subcutaneous fat and connective tissue to create a 6 cm x 4 cm pocket extending toward the spine.
  9. Insert the telemetry device into the subcutaneous pocket and secure it in place using a 2-0 silk suture.
  10. Tunnel the telemetry device antenna under the subcutaneous tissue and secure it in place using a 2-0 silk suture.
  11. Make 1-cm counter skin incisions at the base of the neck, as well as the lower left and upper right chest, for placement of the ECG leads. Tunnel subcutaneously to connect these incisions to the device body pocket and guide the ECG leads to their desired location (Figure 2C).
  12. Place the ECG leads similarly to the steps described above for the femoral implant procedure (section 3).
  13. Create a subcutaneous tunnel from the lateral device pocket to the medial neck incision and thread the two pressure catheters through. Prep these pressure catheters using gel prior to cannulation, as detailed in the femoral implant procedure.
  14. Using a 6-0 polypropylene suture, place a purse-string stitch around the site of cannulation on both vessels and secure with a plastic tourniquet.
  15. Administer a dose of intravenous heparin (100 units/kg) 3 min before cannulation.
  16. Tighten the proximal and distal 2-0 silk tourniquets around the carotid artery. Carefully incise into the vessel at the center of the purse-string stitch using a #11 blade scalpel and dilate slightly with the tip of a curved hemostat.
  17. Insert the pressure catheter corresponding to the LVP channel and advance it into the thoracic ascending aorta, loosening the proximal silk tourniquet to allow for passage of the catheter. Tighten the purse-string suture and tie it around the catheter.
  18. Repeat steps 4.16 and 4.17 for cannulation of the left IJ vein using the pressure catheter corresponding to the BP channel and advance it into the thoracic SVC.
  19. Confirm the appropriate location of the catheter tips in the thoracic SVC and ascending aorta using fluoroscopy (Figure 2D).
  20. Reapproximate the platysma muscle using a 2-0 absorbable suture.
  21. Close the skin with deep dermal and subcuticular sutures using 3-0 and 4-0 absorbable sutures, respectively.

5. Recovery

  1. Discontinue anesthetics. Remove the orogastric tube and extubate when the sheep is breathing without assistance from the ventilator. This typically occurs after the sheep shows signs of arousal (movement, blinking, response to painful stimuli, jaw tone, chewing).
  2. Remove the arterial line.
    NOTE: Continuous blood pressure monitoring can be provided by the telemetry device if one of its pressure catheters has been placed into the aorta.
  3. Transfer the sheep to an isolated housing unit for recovery. Assist the sheep with staying in sternal recumbency and then eventually with standing.
  4. Administer intravenous banamine (2.2 mg/kg) and subcutaneous buprenorphine SR (0.03 mg/kg) for postoperative pain.

Wyniki

Surgical outcomes
A total of 13 sheep underwent single-stage Fontan surgery involving total cavopulmonary connection with detachment of both the SVC and IVC from the right atrium, direct end-to-side anastomosis of the SVC to PA, and placement of an extracardiac conduit between the IVC and PA. Sheep underwent this procedure at a mean age of 13.3 ± 7.6 months. Of these, 3 sheep underwent wireless telemetry device implantation with placement of pressure-sensing catheters into the abdominal aorta ...

Dyskusje

We have developed two surgical methods for the implantation of a wireless telemetry device into an ovine model. The device was successfully implanted in 5 sheep to achieve continuous, long-term monitoring and recording of several cardiovascular parameters, including heart rate, arterial blood pressure, and localized venous pressures from the abdominal IVC and thoracic SVC. All sheep survived the surgery for device implantation without any major complications and went on to undergo a single-stage Fontan operation one mont...

Ujawnienia

This project was funded by the Additional Ventures Cures Collaborative, Palo Alto, California.

Podziękowania

We appreciate the dedicated veterinarian staff at the Animal Research Core. We also wish to express our gratitude to Mary Walker, DVM, MS, for her invaluable expertise and vigilant care throughout the study.

Materiały

NameCompanyCatalog NumberComments
0.9% Sodium Chloride solutionBaxter Healthcare CorporationPharmacyIntraoperative fluid resuscitation and wound rinse
16 G intravenous catheterBD382259For fluid and drug administration
22 G intravascular catheterBD381423For arterial  blood pressure monitoring
70% isopropyl alcoholAspen Vet11795782Topical cleaning solution
ACT cartridgeAbbot Diagnostics03P86-25Activated clotting time
Backhaus towel clampMedlineMDS1411111To affix sterile drape 
BanamineHospira PharmaceuticalsPharmacyPostoperative pain control: concentration 50 mg/mL, dose 2.2 mg/kg
Blood pressure cuffRoyal Philips9.89803E+11Non-invasive blood pressure monitoring
Bupivacaine hydrochlorideHospira PharmaceuticalsPharmacyLocal anesthetic: concentration 2.5 mg/mL, dose 2.5 mg/kg
BuprenorphineHospira PharmaceuticalsPharmacyPostoperative pain control: concentration 0.3 mg/mL, dose 0.03 mg/kg
Castroviejo needle holderMedlineMDS0750386Needle holder when suturing blood vessels
Cautery cleaner padCardinal Health300-2SSTo clean cautery pencil tip
Cautery pencilMedlineESRK3002LFor dissection using electrocautery
CefazolinHospira PharmaceuticalsPharmacyAntibiotic prophylaxis
CetacaineCetylite220Topical anesthetic spray for intubation
ChloraprepBD930825Topical antiseptic
Debakey atraumatic forcepsMedlineMDS1130630FFor tissue handling
DiazepamHospira PharmaceuticalsPharmacySedative: concentration 5 mg/mL, dose 0.5 mg/kg
ECG leads3M2570ECG monitoring
Endotracheal tube, size 8-9Covidien86452, 86114, or 86454To secure airway
Hartmann hemostatic forcepsMedlineMDS1221109To clamp blood vessels and hold small sutures
HeparinHospira PharmaceuticalsPharmacyAnticoagulant: 1,000 USP units/mL
Pressure transducer kitEdwards LifesciencesVSYPX12NFor arterial  blood pressure monitoring
Pulse oximeter lingual clipNellcorPO736For pulse oximetry
IsofluraneBaxter Healthcare CorporationPharmacyAnesthetic: dose 1-3%
Kantrowitz forcep (right angle)MedlineMDS1243528For blunt dissection around blood vessels
KetamineHospira PharmaceuticalsPharmacySedative: concentration 100 mg/mL, dose 4 mg/kg
Laparotomy drapeMedlineDYNJP3008Sterile drape
Lubricating jellyMedlineMDS0322273ZEndotracheal tube lubricant
Mayo Hegar needle holderMedlineMDS2418420FNeedle holder when suturing soft tissue
Mayo scissorsMedlineMDS0816121To cut suture
Metzenbaum curved scissorsMedlineMDS3223226For sharp dissection
Needles and syringesCardinal Health309604For intravenous and subcutaneous drug administration 
OptixcareAventixOPX-4252Corneal lubricant
Perma-Hand silk sutureEthiconC016DFor blood vessel ligation and attachment of the telemetry device subcutaneously
PhysioTel Digital wireless telemetry deviceData Sciences InternationalL21 modelWireless telemetry device implant
Pierce microforcepsMedlineMDG384908Small needle handling 
Plastic tourniquet and suture snareMedtronic 79013To facilitate hemostasis during vessel cannulation
Pressure bagCarefusion64-10029For arterial blood pressure monitoring
Prolene 6-0 sutureEthicon8307HPurse string stitch for vessel cannulation
PropofolFresenius KabiPharmacyAnesthetic: concentration 10 mg/mL, dose 20-45 mg/kg/h
Scalpel #10 bladeMedlineMDS15310For skin incisions
Scalpel #11 bladeMedlineCISION11CSFor incision into blood vessels
Schnidt tonsil forcepsMedlineMDS5018719For blunt dissection through subcutaneous tissue
SoftCarry stretcherFour Flags Over AspenSSTR-4For animal transportation
Sterile disposable OR towelMedlineMDT2168201Sterile drape
Sterile bowlLSL Industries5232To hold saline solution
Sterile cotton X-ray detectable gauze spongeMedlineNON21430LFFluid absorption
Orogastric tubeJorgensen Lab, Inc.J0348RFor stomach and rumen decompression
T-portMedlineDYNDTN0001Intravenous catheter tubing connector
Urine drainage bagCovidien3512Connects to orogastric tube to collect gastric fluids
Veterinary trocar with styletBraintree Scientific, Inc.TRO-STY 7B-12To guide telemetry wires through subcutaneous tissue
Vicryl 2-0 sutureEthiconVCPB269HClosure of subcutaneous soft tissue
Vicryl 3-0 sutureEthiconVCPB416HClosure of deep dermal layer
Vicryl 4-0 sutureEthiconJ494HCloser of subcuticular layer
Warming blanketJorgensen Lab, Inc.J1034BTo maintain animal's body temperature
Weitlander retractorTeleflex Medical165358For wound retraction
Yankauer bulb tip suctionMedlineDYND50138Sterile waste management

Odniesienia

  1. Fontan, F. Baudet, E. Surgical repair of tricuspid atresia. Thorax. 26 (3), 240-248 (1971).
  2. Attanavanich, S., Limsuwan, A., Vanichkul, S., Lertsithichai, P., Ngodngamthaweesuk, M. Single-stage versus two-stage modified fontan procedure. Asian Cardiovasc Thorac Ann. 15 (4), 327-331 (2007).
  3. Bove, E. L. Lloyd, T. R. Staged reconstruction for hypoplastic left heart syndrome. Contemporary results. Ann Surg. 224 (3), 387-394; discussion 394-385 (1996).
  4. Iskander, C. et al. Comparison of morbidity and mortality outcomes between hybrid palliation and norwood palliation procedures for hypoplastic left heart syndrome: Meta-analysis and systematic review. J Clin Med. 13 (14), 4244 (2024).
  5. Salik, I., Mehta, B., Ambati, S. Bidirectional Glenn Procedure or Hemi-Fontan. Statpearls, Treasure Island, FL (2024).
  6. Daley, M. D'udekem, Y. The optimal Fontan operation: Lateral tunnel or extracardiac conduit? J Thorac Cardiovasc Surg. 162 (6), 1825-1834 (2021).
  7. Jalal, Z. et al. Role and applications of experimental animal models of Fontan circulation. J Clin Med. 13 (9), 2601 (2024).
  8. Al Balushi, A. Mackie, A. S. Protein-losing enteropathy following Fontan palliation. Can J Cardiol. 35 (12), 1857-1860 (2019).
  9. Emamaullee, J. et al. Fontan-associated liver disease: Screening, management, and transplant considerations. Circulation. 142 (6), 591-604 (2020).
  10. Mazza, G. A., Gribaudo, E., Agnoletti, G. The pathophysiology and complications of Fontan circulation. Acta Biomed. 92 (5), e2021260 (2021).
  11. Schwartz, I., Mccracken, C. E., Petit, C. J., Sachdeva, R. Late outcomes after the Fontan procedure in patients with single ventricle: A meta-analysis. Heart. 104 (18), 1508-1514 (2018).
  12. Zafar, F. et al. Long-term kidney function after the Fontan operation: Jacc review topic of the week. J Am Coll Cardiol. 76 (3), 334-341 (2020).
  13. Van Puyvelde, J. et al. Creation of the Fontan circulation in sheep: A survival model. Interact Cardiovasc Thorac Surg. 29 (1), 15-21 (2019).
  14. Cysyk, J. et al. Chronic in vivo test of a right heart replacement blood pump for failed Fontan circulation. ASAIO J. 65 (6), 593-600 (2019).
  15. Cysyk, J. P. et al. Miniaturized Fontan circulation assist device: Chronic in vivo evaluation. ASAIO J. 67 (11), 1240--1249 (2021).
  16. D'udekem, Y. et al. Validating the concept of mechanical circulatory support with a rotary blood pump in the inferior vena cava in an ovine Fontan model. Bioengineering (Basel). 11 (6), 594 (2024).
  17. Granegger, M. et al. Feasibility of an animal model for cavopulmonary support with a double-outflow pump. ASAIO J. 69 (7), 673-680 (2023).
  18. Wei, X. et al. Mechanical circulatory support of a univentricular Fontan circulation with a continuous axial-flow pump in a piglet model. ASAIO J. 61 (2), 196-201 (2015).
  19. Zhu, J. et al. Cavopulmonary support with a microaxial pump for the failing Fontan physiology. ASAIO J. 61 (1), 49-54 (2015).
  20. Kelly, J. M. et al. Investigation of a chronic single-stage sheep Fontan model. JTCVS Open. 21, 268-278 (2024).
  21. Anderson, N. H. et al. Telemetry for cardiovascular monitoring in a pharmacological study: New approaches to data analysis. Hypertension. 33 (1 Pt 2), 248-255 (1999).
  22. Kearney, K., Appleby, C., Kieper, J., Atterson, P. Comparative analysis of data sciences international PhysioTel™ D70 and PhysioTel™ digital telemetry platforms. J Pharmacol Toxicol Methods. 81, 364-365 (2016).
  23. Physiotel digital l series. At <https://www.datasci.com/products/implantable-telemetry/large-animal/physiotel-digital-l > (2024).

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