Name: chronic ovine model of right ventricular failure and functional tricuspid regurgitation
Uploaded: 2023-03-17T13:40:00
Description: Watch this Scientific Journal Video about Chronic Ovine Model of Right Ventricular Failure and Functional Tricuspid Regurgitation at JoVE.com

The study was funded by an internal grant from the Meijer Heart and Vascular Institute at Spectrum Health.

The protocol was approved by the Michigan State University Institutional Animal Care and Use Committee (IACUC) (Protocol 2020-035, approved on 7/27/2020). For this study, 20 adult male sheep weighing 62 &#177; 7 kg were used.
1. Preoperative steps
<ol>
	<li>Fast the animal 12 h prior to surgery (overnight).</li>
	<li>Place the animal in a sheep chair (Figure 1), and prepare for the right jugular vein cannulation using a long 11 Fr introducer she...

<ol>
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M., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=2020+ACC/AHA+Guideline+for+the+Management+of+Patients+With+Valvular+Heart+Disease:+Executive+summary:+A+report+of+the+American+College+of+Cardiology/American+Heart+Association+Joint+Committee+on+Clinical+Practice+Guidelines.">2020 ACC/AHA Guideline for the Management of Patients With Valvular Heart Disease: Executive summary: A report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines.</a> Circulation. 143 (5), 35-71 (2021).</li><li>Vonk-Noordegraaf, A., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Right+heart+adaptation+to+pulmonary+arterial+hypertension:+physiology+and+pathobiology.">Right heart adaptation to pulmonary arterial hypertension: physiology and pathobiology.</a> Journal of the American College of Cardiology. 62, 22-33 (2013).</li><li>Yoganathan, A., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Tricuspid+valve+diseases:+Interventions+on+the+forgotten+heart+valve.">Tricuspid valve diseases: Interventions on the forgotten heart valve.</a> Journal of Cardiac Surgery. 36 (1), 219-228 (2021).</li><li>Vachi&#233;ry, J. 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M., Coghlan, G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Characterizing+the+right+ventricle:+Advancing+our+knowledge.">Characterizing the right ventricle: Advancing our knowledge.</a> American Journal of Cardiology. 110, 3-8 (2012).</li><li>Malinowski, M., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Large+animal+model+of+acute+right+ventricular+failure+with+functional+tricuspid+regurgitation.">Large animal model of acute right ventricular failure with functional tricuspid regurgitation.</a> International Journal of Cardiology. 264, 124-129 (2018).</li><li>Borgdorff, M. A., Dickinson, M. G., Berger, R. M., Bartelds, B. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Right+ventricular+failure+due+to+chronic+pressure+load:+What+have+we+learned+in+animal+models+since+the+NIH+working+group+statement.">Right ventricular failure due to chronic pressure load: What have we learned in animal models since the NIH working group statement.</a> Heart Failure Review. 20 (4), 475-491 (2015).</li><li>Andersen, A., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Animal+models+of+right+heart+failure.">Animal models of right heart failure.</a> Cardiovascular Diagnosis and Therapy. 10 (5), 1561-1579 (2020).</li><li>Dixon, J. A., Spinale, F. G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Large+animal+models+of+heart+failure:+A+critical+link+in+the+translation+of+basic+science+to+clinical+practice.">Large animal models of heart failure: A critical link in the translation of basic science to clinical practice.</a> Circulation: Heart Failure. 2 (3), 262-271 (2009).</li><li>Miyagi, C., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Large+animal+models+of+heart+failure+with+preserved+ejection+fraction.">Large animal models of heart failure with preserved ejection fraction.</a> Heart Failure Review. 27 (2), 595-608 (2022).</li><li>Sato, H., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Large+animal+model+of+chronic+pulmonary+hypertension.">Large animal model of chronic pulmonary hypertension.</a> American Society for Artificial Internal Organs Journal. 54 (4), 396-400 (2008).</li><li>Bogaard, H. J., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Chronic+pulmonary+artery+pressure+elevation+is+insufficient+to+explain+right+heart+failure.">Chronic pulmonary artery pressure elevation is insufficient to explain right heart failure.</a> Circulation. 120 (20), 1951-1960 (2009).</li><li>Xie, X. J., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Tricuspid+leaflet+resection+in+an+open+beating+heart+for+the+creation+of+a+canine+tricuspid+regurgitation+model.">Tricuspid leaflet resection in an open beating heart for the creation of a canine tricuspid regurgitation model.</a> Interactive Cardiovascular and Thoracic Surgery. 22 (2), 149-154 (2016).</li><li>Hoppe, H., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Percutaneous+technique+for+creation+of+tricuspid+regurgitation+in+an+ovine+model.">Percutaneous technique for creation of tricuspid regurgitation in an ovine model.</a> Journal of Vascular and Interventional Radiology. 18, 133-136 (2007).</li><li>Malinowski, M., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Large+animal+model+of+functional+tricuspid+regurgitation+in+pacing+induced+end-stage+heart+failure.">Large animal model of functional tricuspid regurgitation in pacing induced end-stage heart failure.</a> Interactive Cardiovascular and Thoracic Surgery. 24 (6), 905-910 (2017).</li><li>Ukita, R., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=A+large+animal+model+for+pulmonary+hypertension+and+right+ventricular+failure:+Left+pulmonary+artery+ligation+and+progressive+main+pulmonary+artery+banding+in+sheep.">A large animal model for pulmonary hypertension and right ventricular failure: Left pulmonary artery ligation and progressive main pulmonary artery banding in sheep.</a> Journal of Visualized Experiments. (173), e62694 (2021).</li><li>Dufva, M. J., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Pulmonary+arterial+banding+in+mice+may+be+a+suitable+model+for+studies+on+ventricular+mechanics+in+pediatric+pulmonary+arterial+hypertension.">Pulmonary arterial banding in mice may be a suitable model for studies on ventricular mechanics in pediatric pulmonary arterial hypertension.</a> Journal of Cardiovascular Magnetic Resonance. 23 (1), 66 (2021).</li><li>Verbelen, T., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Mechanical+support+of+the+pressure+overloaded+right+ventricle:+An+acute+feasibility+study+comparing+low+and+high+flow+support.">Mechanical support of the pressure overloaded right ventricle: An acute feasibility study comparing low and high flow support.</a> American Journal of Physiology-Heart and Circulatory Physiology. 309 (4), 615-624 (2015).</li></ol>

In this model, 8 weeks of pulmonary artery banding resulted in a stable chronic ovine model of right ventricular dysfunction and, in most cases, significant FTR. The strengths of the presented chronic PAB model include the precise afterload adjustment during the procedure, although its influence on RV responses may differ. The model is suitable for evaluating varying degrees of RV failure or FTR, with the severity modulated by the degree of pulmonary artery constriction. Moreover, the application of fixed and stable resi...

Right ventricular failure (RVF) is recognized as an important factor contributing to the morbidity and mortality of cardiac patients. The most common causes of RVF are left-sided heart disease and pulmonary hypertension1. During the progression of RVF, functional tricuspid regurgitation (FTR) may arise as a consequence of right ventricular (RV) dysfunction, annular dilatation, and subvalvular remodeling. Moderate to severe FTR is an independent predictor of mortality2,3, and it is estimated that 80%-90% of tricuspid regurgitation cases are functional in nature4. FTR itself may promote adverse ventricular remodeling by influencing either afterload or preload5. The tricuspid valve has historically been considered the forgotten valve6, and it was believed that the treatment of left-sided heart disease would resolve the associated RV pathology and FTR7. Recent data have shown this to be a faulty strategy, and current clinical guidelines advocate a much more aggressive approach to FTR4. However, the pathophysiology of severe FTR associated with right ventricular dysfunction is still poorly understood, leading to suboptimal clinical results8. The currently available large animal models of RVF are based on pressure, volume, or mixed overload. We have previously described a large animal model of RVF and TR but only in an acute setting9.
The current study focuses on a chronic ovine model of pulmonary artery banding (PAB) to increase RV afterload (pressure overload) and induce RV dysfunction and FTR. The afterload model is reliable and reproducible compared to pulmonary hypertension models, in which changes in microvasculature are less predictable and more likely10. The goal of the study was to develop a chronic large animal model of RVF and FTR that would most accurately mimic RV pressure overload in patients with left-sided heart disease and pulmonary hypertension. The establishment of such a model would permit in-depth studies on the pathophysiology of the ventricular and valvular remodeling associated with RV dysfunction and tricuspid insufficiency. The ovine model was chosen based on our prior work on the mitral valve and the published literature supporting the anatomical and physiological similarities between human and ovine hearts11,12,13.
For this study, 20 adult sheep (62 &#177; 7 kg) underwent a left thoracotomy and main pulmonary artery banding (PAB) to at least double the systolic pulmonary artery pressure (SPAP), thus inducing RV pressure overload. The animals were followed for 8 weeks, and the symptoms of heart failure were treated with diuretics when clinically apparent. Surveillance echocardiography was performed periodically to assess RV function and valvular competence. Following the completion of the experimental protocol for model development (8 weeks), the animals were taken back to the operating room for median sternotomy and the implantation of sonomicrometry crystals on the epicardial and intra-cardiac structures. This procedure was performed using cardiopulmonary bypass with the heart beating and with bicaval control. There were no problems in weaning the animals from the cardiopulmonary bypass or acquiring the sonomicrometry data in a stable steady-state hemodynamic environment without the need for inotropes for right heart support. We anticipate performing tricuspid ring annuloplasty and other right heart procedures in the near future using a right thoracotomy approach in both terminal and survival experiments. The current experience leads us to believe that it will be possible to wean the animals from the cardiopulmonary bypass without difficulty and that long-term survival is feasible. As such, we believe the model will permit the performance of clinically pertinent cardiac procedures. Below is a description of the steps (perioperative and operative) performed for carrying out the ovine experimental protocol.

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	<tbody>
		<tr>
			<td>Anesthesia Machine Drager Narkomed MRI-2</td>
			<td>Drager</td>
			<td>4116091-001</td>
			<td></td>
		</tr>
		<tr>
			<td>angiocatheter</td>
			<td>BD</td>
			<td>BD382268</td>
			<td>14GAx8.25cm</td>
		</tr>
		<tr>
			<td>BD ChloraPrep Scrub Teal 26 ml applicator with a sterile solution</td>
			<td></td>
			<td></td>
			<td></td>
		</tr>
		<tr>
			<td>Blade #11</td>
			<td>Bard-Parker</td>
			<td>371111</td>
			<td></td>
		</tr>
		<tr>
			<td>Buprenorphine&#160;</td>
			<td>HIKMA</td>
			<td></td>
			<td></td>
		</tr>
		<tr>
			<td>cefazolin 1.0g</td>
			<td>Hikma</td>
			<td>0143-9924-90</td>
			<td></td>
		</tr>
		<tr>
			<td>Diprivan 200mg/20ml</td>
			<td>63323-0269-29</td>
			<td>FRESENIUS KABI</td>
			<td></td>
		</tr>
		<tr>
			<td>Electrosurgical generator Valleylab Force FX</td>
			<td>Valleylab</td>
			<td>CF5L44233A</td>
			<td></td>
		</tr>
		<tr>
			<td>Gentamicin Sulfate 40 mg / mL</td>
			<td>Fresenius</td>
			<td>406365</td>
			<td></td>
		</tr>
		<tr>
			<td>i-Stat Blood analyzer MN 300</td>
			<td>Abbott</td>
			<td></td>
			<td></td>
		</tr>
		<tr>
			<td>Lidocaine HCl 1%</td>
			<td>Pfizer</td>
			<td>243243</td>
			<td></td>
		</tr>
		<tr>
			<td>Open ligating clip appliers Horizon Medium</td>
			<td>Teleflex</td>
			<td>237061</td>
			<td></td>
		</tr>
		<tr>
			<td>PERMAHAND Silk Suture</td>
			<td>PERMA HAND</td>
			<td>SA 63H</td>
			<td></td>
		</tr>
		<tr>
			<td>Pinnacle Introducer sheath</td>
			<td>Terrumo</td>
			<td>RSS102</td>
			<td>sheath length 10cm</td>
		</tr>
		<tr>
			<td>Prolene 3-0</td>
			<td>ETHICON</td>
			<td>8684H</td>
			<td></td>
		</tr>
		<tr>
			<td>Titanium Clips Medium</td>
			<td>Teleflex</td>
			<td>2200</td>
			<td></td>
		</tr>
		<tr>
			<td>Umbilical tape</td>
			<td>Ethicon</td>
			<td>EFA 1165</td>
			<td></td>
		</tr>
		<tr>
			<td>VICRYL 2 coated undyed 1X54&#34; TP-1</td>
			<td>ETHICON</td>
			<td>J 880T</td>
			<td></td>
		</tr>
		<tr>
			<td>Vicryl 2-0</td>
			<td>ETHICON</td>
			<td>J269H</td>
			<td></td>
		</tr>
	</tbody>
</table>

chronic ovine model of right ventricular failure and functional tricuspid regurgitation

The pathophysiology of severe functional tricuspid regurgitation (FTR) associated with right ventricular dysfunction is poorly understood, leading to suboptimal clinical results. We set out to establish a chronic ovine model of FTR and right heart failure to investigate the mechanisms of FTR. Twenty adult male sheep (6-12 months old, 62 &#177; 7 kg) underwent a left thoracotomy and baseline echocardiography. A pulmonary artery band (PAB) was placed and cinched around the main pulmonary artery (PA) to at least double the systolic pulmonary artery pressure (SPAP), inducing right ventricular (RV) pressure overload and signs of RV dilatation. PAB acutely increased the SPAP from 21 &#177; 2 mmHg to 62 &#177; 2 mmHg. The animals were followed for 8 weeks, symptoms of heart failure were treated with diuretics, and surveillance echocardiography was used to assess for pleural and abdominal fluid collection. Three animals died during the follow-up period due to stroke, hemorrhage, and acute heart failure. After 2 months, a median sternotomy and epicardial echocardiography were performed. Of the surviving 17 animals, 3 developed mild tricuspid regurgitation, 3 developed moderate tricuspid regurgitation, and 11 developed severe tricuspid regurgitation. Eight weeks of pulmonary artery banding resulted in a stable chronic ovine model of right ventricular dysfunction and significant FTR. This large animal platform can be used to further investigate the structural and molecular basis of RV failure and functional tricuspid regurgitation.

Following the completion of the experimental protocol for model development (nearly 8 weeks), the animals were taken back to the operating room for median sternotomy and the implantation of sonomicrometry crystals on the epicardial and intra-cardiac structures. This procedure was performed using cardiopulmonary bypass with the heart beating and with bicaval control, as&#160;described by our group in detail previously9. There were no problems in weaning the animals from the cardiopulmonary bypass o...

Watch this Scientific Journal Video about Chronic Ovine Model of Right Ventricular Failure and Functional Tricuspid Regurgitation at JoVE.com

Chronic Ovine Model of Right Ventricular Failure and Functional Tricuspid Regurgitation

Right ventricular failure and functional tricuspid regurgitation are associated with left-sided heart disease and pulmonary hypertension, which contribute significantly to morbidity and mortality in patients. Establishing a chronic ovine model to study right ventricular failure and functional tricuspid regurgitation will help in understanding their mechanisms, progression, and possible treatments.

The pathophysiology of severe functional tricuspid regurgitation (FTR) associated with right ventricular dysfunction is poorly understood, leading to ...

The model is similar to those previously described in the literature. Although our specific goal was to induce significant functional tricuspid regurgitation rather than just isolated right heart dysfunction. The technique may be used in the future to study mechanisms of functional tricuspid regurgitation with its associated right ventricular annular and subular remodeling, as well as tissue changes.The model may be helpful in identifying molecular pathways responsible for functional tricuspid regurgitation and establishing more efficient and complex surgical techniques for its treatment. Begin by placing the animal in a sheep chair. Shave the right anterior aspect of the neck around 10 to 15 centimeters lateral from the midline for the right jugular vein using clippers.After disinfecting the surgical area, turn the animal's head to the left to expose the right anterior and lateral aspects of the neck. Then localize the jugular vein course by compressing the bottom of the neck to distend the vein. Now, anesthitize the insertion site with 1%lidocaine.Using a number 11 blade, cut the skin above and perpendicular to the vein and cannulate with a 14 gauge angio catheter. Once the angio catheter is in place, remove the needle, pass the guide wire, followed by removing the catheter. Then, place the 11 french sheath and remove the guide wire before securing the sheath.Ensure the patency and proper placement of the cannula by withdrawing dark red blood and performing a saline flush to confirm the flow and absence of swelling at the insertion site. After inducing propofol intravenously, intubate with an endotracheal tube using a laryngoscope with a number five blade as described in the manuscript. Confirm proper placement by the bilateral breath sounds and condensation on the endotracheal tube.After preparing the operative field, shave the left anterior thorax. Then, apply sterile drapes around the disinfected surgical area. Make a 10 centimeter long skin and subcutaneous incision at the level of the fourth intercostal space.Confirm the correct intercostal space is incised by identifying the thoracic inlet and counting the intercostal spaces downward. Subsequently, continue the incision in the center and along the fourth intercostal space. Now, divide the intercostal muscles, open the chest cavity and spread the ribs with a mini thoracotomy finochietto style retractor.Avoid injuring the left internal mammary artery at the sternal border of the incision and the lung at the superior border. Then, perform baseline epicardial echocardiography to assess the biventricular function and valvular competence. Identify the left internal mammary artery at the sternal border of the incision, remove the adjacent tissues around it, and prepare to establish an arterial line for pressure monitoring.Now, place two 4-0 silk sutures around the artery with one proximal and one distal to the cannulation site. Use titanium clips with a clip applier to clip the left internal mammary artery distal to the planned cannulation site to prevent backflow bleeding during cannulation. Make a perpendicular incision that is half of the circumference of the catheter in the left internal mammary artery with a number 11 blade.Insert an 18 gauge angio catheter and attach it to the arterial line module. When proper placement of the angio catheter is confirmed by arterial pressure line reading, secure the catheter using two 4-0 silk sutures placed earlier. Next, perform pericardiotomy starting at the level of pulmonary artery sinuses and going four to five centimeters laterally along the main pulmonary artery taking care not to injure the left phrenic nerve.Apply four to five retraction stitches to the opened pericardium to create a pericardial well which facilitates exposure and dissection between the pulmonary trunk and aorta. Using blunt right angle forceps, dissect the main pulmonary artery from ascending aorta around two to three centimeters from its origin as described in the manuscript. To separate the main pulmonary artery from the ascending aorta, use electrocautery or scissors to remove the connective tissue between the two structures.Pass an umbilical tape around the main pulmonary artery with a blunt right angle clamp. Then establish a main pulmonary artery pressure line by placing a 5-0 monofilament purse string suture one centimeter distal from the main pulmonary artery sinuses. Insert a 20 gauge angio catheter and connect it to a monitoring line.Before cinching the umbilical tape, ensure correct main pulmonary artery and arterial line readings are achieved. After holding both ends of the umbilical tape, clip them together to reduce the lumen of the main pulmonary artery. Then, tighten the band with the successive application of a clip applier as described in the manuscript.Perform post banding echocardiography to assess the biventricular function and valvular competence as demonstrated earlier. Remove the main pulmonary artery pressure line. When maximal cinching and stable hemodynamic conditions are achieved, secure the umbilical tape to the adventitia of the main pulmonary artery using a 5-0 monofilament suture to avoid distal migration.Then, remove the arterial line and ensure good hemostasis by checking for any bleeding from the area where the band and arterial lines were placed. Place a chest tube in the left thorax with the entry site one intercostal space below the initial incision. Close the ribs with two vicryl 2-0 sutures and close the wound with three layer continuous sutures.Vicryl 2-0 for the muscle and subcutaneous tissues and proline 3-0 for the skin. Once good hemostasis is confirmed, remove the chest tube and extubate the animal. After the follow-up period, the mean TR grade increased from 0.4 to 3.2, demonstrating signs of evolving right ventricular failure and the development of significant TR after eight weeks of pulmonary banding.Consistent with the echocardiographic examination. Over or under tightening of the band may result in the early animal demise or not inducing redicular failure and functional tricuspid regurgitation. Additional methods inducing heart failure may be performed after initial made pulmonary artery banding, like ventricle art pacing or ascending aorta banding, or band may be released to elevate right heart failure.

Research

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