Prepared Pulmonary venous Orifice

HOW TO DO IT The Surgical Technique of Heterotopic Heart Transplantation D. Novitzky, M.D., F.C.S.(S.A.), D. K. C. Cooper, M.A., M.B., B.S., Ph.D., F.R.C.S., and C. N. Barnard, M.D., M.Med., M.S., Ph.D., F.A.C.S., F.A.C.C., D.Sc. (Hon Causa) ABSTRACT The surgical technique of heterotopic heart transplantation is detailed and illustrated. The donor heart is excised after cardioplegic arrest and topical cooling; its preparation and implantation in the recipient are described. Emphasis is placed on ensuring nonrestrictive anastomoses between the left and right atria of the recipient and the donor, on estimating the optimal length of the donor aorta, and on the insertion of a prosthetic graft between the donor and the recipient pulmonary arteries. Fortysix such transplants have been performed to date without operative or early postoperative mortality related to technical problems. Heterotopic heart transplantation has a long history in the experimental laboratory [l] but was not attempted clinically until 1974 [2]. Based on extensive experimental work [3], a form of heterotopic transplantation was carried out whereby the donor heart acted solely as a left ventricular assist device [2]. Two such operations were performed, after which the technique was modified to allow bypass and support of both recipient ventricles [2]. Heterotopic heart transplantation has several advantages and some disadvantages as compared with orthotopic transplantation; these have been discussed elsewhere [4, 5, 61. Fortysix such operations have been performed in our unit, including four retransplants [4, 5, 71, but few other centers involved in heart transplantation have performed this operation. This may result in part from lack of familiarity with the various technical steps of the procedure (which is a little more complex than orthotopic trans- From the Department of Cardiac Surgery, Groote Schuur Hospital and University of Cape Town Medical School, Cape Town, Republic of South Africa. Accepted for publication Nov 6, 1982. Address reprint requests to Dr. Novitzky, Department of Cardiac Surgery, University of Cape Town Medical School, Cape Town, Republic of South Africa. plantation), because a detailed account of the operative technique has not yet been published, to our knowledge. In this report we present details of the technique of heterotopic heart transplantation, based on our experience at Groote Schuur Hospital. Donor Heart Excision With the subject supine, a median sternotomy is performed and the pericardium opened longitudinally. The heart is inspected for external signs of intracardiac abnormalities and, where applicable, for damage caused by trauma or external cardiac massage. A pursestring suture is placed in the ascending aorta for subsequent insertion of a cardioplegia catheter. The superior vena cava (SVC) is mobilized along the whole of its length and two ligatures are passed around it cranial to the azygos vein, though these ligatures are not tied down at this stage. The azygos vein is doubly ligated and divided. A tape is passed around the inferior vena cava (IVC). The donor is fully heparinized. A cardioplegia catheter is inserted into the ascending aorta. The SVC is doubly ligated as high as possible and divided. The IVC is cross-clamped at the diaphragm and divided immediately superior to the clamp; this decompresses the right side of the heart. The left side is decompressed by opening a right pulmonary vein with scissors. A cross-clamp is applied to the aorta distal to the cardioplegia line at the level of the innominate artery. Sufficient cold cardioplegic agent is given rapidly to ensure arrest of the heart; between 400 ml and 1 liter is usually required. A check is made on the ascending aorta (by palpation) to ensure that the intraluminal pressure does not rise too high (less than 100 mm Hg). Cold saline solution at 4 C is poured over the heart to fill the pericardial cavity. After the cardioplegic agent has been ad- 476

477 How to Do It: Novitzky, Cooper, and Barnard: Heterotopic Heart Transplantation ministered, the topical saline is sucked out and section of the right pulmonary veins is completed, together with division of the left pulmonary veins. The left and right pulmonary arteries are divided, and the aorta is transected immediately proximal to the cross-clamp. The apex of the heart is then lifted anteriorly, and the mediastinal tissue posterior to the atria and major vessels is divided by sharp dissection, allowing the heart to be removed from the pericardial cavity. The approximate time from ligation of the SVC to completion of excision of the heart is 6 to 10 minutes. Preparation of the Donor Heart The heart is placed in a bowl containing saline or cardioplegic solution at 4"C, where it is prepared for implantation into the recipient (Fig 1). The orifices of both right pulmonary veins and of the IVC are closed with continuous, doublelayered sutures of 5-0 polypropylene, with care being taken to ensure that coronary sinus drainage is not occluded during closure of the IVC. The bridge of tissue between the left superior and inferior pulmonary veins is excised to make a single opening into the left atrium; this opening may need to be extended to achieve a diameter of approximately 3.5 to 4 cm, or the equivalent of a normal mitral valve orifice. The midpoint of the posterior wall of this opening is marked with a suture as a reference during subsequent implantation into the recipient. The main pulmonary artery is divided at its bifurcation. A longitudinal 5 cm incision, just to the right of the interatrial septum, is made in the posterior aspect of the SVC and right atrium; at least half the length of this incision must involve the right atrial wall. Preparing the heart in this way requires 15 to 20 minutes. The organ is then transferred to the surgical team, which has been preparing the recipient simultaneously. Preparation of the Recipient With the patient supine, a midline sternotomy is performed and the pericardium opened longitudinally. A right-sided pleuropericardial flap is created (Fig 2), first by dividing the mediastinal pleura immediately posterior to the sternum Prepared Pulmonary venous Orifice -%t- Azygos SVC-RA incision R. PVs [sutured] IVC [sutured] Fig 1. Posterior view of donor heart prepared for implantation. (A0 = aorta; SVC = superior vena cava; SVC- RA = superior vena caval-right atrial; R.PVs = right pulmonary veins; IVC = inferior vena cava; RV = right ventricle; LV = left ventricle; CS = coronary sinus; LA = left atrium; PA = pulmonary artery.). Line of reflection of pleu;o-""". pericardial flap R Phrenic nerve Line of incision of pleuro-pertcardial flap Fig 2. Right-sided view of rnediastinum of recipient. The line of the pleuropericardial incision is indicated. and then by extending this incision medially over the diaphragm to a point 2 cm from the right phrenic nerve; a similar reflection of the pleuropericardium is made superiorly, extending the incision toward the SVC, again taking care to avoid the phrenic nerve. In this way a rectangular flap is created that comprises the parietal pericardium and mediastinal pleura. Hemostasis of the edges of this flap must be carried out carefully, because no further opportunity to do this will arise. The flap is allowed to fall back into the right lung (Fig 3), creating a single large right pleuropericardial cavity. The patient is fully heparinized. An aortic

478 The Annals of Thoracic Surgery Vol 36 No 4 October 1983 N. in LA Reflected pleuro-pericardial flap Fig 3. Reflection of pleuropericardial flap to lie anterior to the hilum of right lung of recipient. (RA = right atrium; RV = right ventricle; LA = left atrium; N = nerve.) DONOR 3 v '$4 RECIPIENT L L, d Fig 4. Donor and recipient hearts, showing the beginning of the posterior suture line of the left atrial anastomosis. (See Fig 1 for other abbreviations.) cannula is inserted at the level of the origin of the innominate artery, and venous cannulas are inserted into the SVC (through the right atrial appendage) and the IVC (through the low atrial wall). Cardiopulmonary bypass is initiated and a left ventricular apical vent introduced. The patient is cooled to 28 C. For most open-heart procedures our cardiopulmonary bypass system includes two suction catheters and one ventricular suction vent, which return blood to the pump oxygenator; for heterotopic heart transplantation we have available four suction catheters and two vents. Anas tomos is of Left Atria An incision, as for mitral valve surgery, is made into the recipient left atrium immediately posterior to the interatrial groove, extending from the superior to the inferior extremes of the groove (Fig 4). The donor heart is then placed in the right thoracic cavity anterior to the collapsed right lung and lying alongside the recipient heart. The midpoint of the posterior lip of the incision in the recipient left atrium is sutured using double-ended 4-0 polypropylene to the midpoint of the posterior lip of the donor left atrium at the site of the previously inserted marker stitch (see Fig 4). The two atria are anastomosed by a continuous suture, first along the posterior aspect and then along the anterior aspect (Fig 5). The completed anastomosis will be I Fig 5. Completed anterior left atrial suture line. A left ventricular vent has been inserted in the donor heart. The superior vena caval-right atrial (SVC-RA) incision in each heart is shown. Note that the inferior point of the incision in the donor SVC-RA area (A) will be sutured to the midpoint in the posterior lip of the incision in the recipient SVC-RA area (a). totally inaccessible at the end of the operation, and therefore it is essential that it be hemostatic. A wide communication between the two left atria has been created, forming a common atrium from which blood can enter either donor or recipient left ventricles. An apical vent is introduced into the donor left ventricle, and gentle suction is applied to help prevent myocardial rewarming by recipient blood.

479 How to Do It: Novitzky, Cooper, and Barnard: Heterotopic Heart Transplantation Fig 6. The first stitch in the anastomosis between the SVC-RA areas of the donor and the recipient has been inserted, as indicated by points A and a. Donor Myocardial Protection Between the performance of each anastomosis, cold saline solution (4 C) is poured over the donor heart as it lies in the right pleural cavity to maintain an adequate state of myocardial hypothermia. This continues until the donor heart is revascularized. Further increments of cold cardioplegic solution can be infused into the donor ascending aorta, but we believe that excessive pharmacological cardioplegia may lead to delayed resumption of myocardial contractions on rewarming; additional cardioplegic agent should only be administered if there is evidence of myocardial contractile activity. Once infusion of cardioplegic solution has begun and all air has been displaced from the aorta, a crossclamp is applied to occlude the distal end of this vessel, thus ensuring that the donor coronary arteries are adequately perfused. Anastomosis of Right Atria Clamps or snares are placed around the SVC and IVC. A 5 cm longitudinal incision is made into the lateral aspect of the recipient SVC and right atrium just anterior to the interatrial groove, beginning 2 to 3 cm above the junction of the vena cava and the right atrium and continuing 2 to 3 cm into the right atrium (see Fig 5). Coronary venous return must be drained to 3 Fig 7. The SVC-RA anterior suture line has been completed, and the aortic anastomosis begun. (A0 = aorta; PA = pulmonary artery.) prevent the blood from obscuring the operative field, although it is sometimes possible to leave the IVC unsnared, thus allowing drainage of coronary sinus blood into the IVC cannula. The donor SVC is extended alongside its counterpart. An eyelid retractor is used to retract the anterior lip of the incision in the recipient right atrium. The midpoint of the posterior lip of the incision in the recipient atrium is sutured to the most caudal point of the incision in the donor atrium, using a double-ended 5-0 polypropylene suture (Fig 6). The two right atria are then anastomosed by a continuous suture carried in each direction, first posteriorly and then anteriorly. At the completion of this anastomosis the ligated donor azygos vein remnant will lie at the midpoint of the anterior suture line (Fig 7), over which a small metal ring is tied down as a fluoroscopic reference for the passage of endomyocardial biopsy forceps into the donor heart after operation. The maneuver of suturing the midpoint of the posterior lip of the recipient atrial wall to the most inferior aspect of the incision in the donor atrium ensures that this anastomosis will remain wide, allowing free flow of blood from one chamber to the other

480 The Annals of Thoracic Surgery Vol 36 No 4 October 1983 The sidebiting clamp is removed from the recipient aorta, and from this point the donor myocardium is perfused continuously with blood from the pump oxygenator. To avoid continuous spillage of blood into the surgical field, a sucker is introduced into the donor pulmonary artery (Fig 8). The patient can now be rewarmed slowly to 37 C. Fig 8. Completion of the aortic anastomosis. The recipient pulmonary artery is incised and anastomosis of the Dacron graft begun. and permitting easy passage of the endomyocardial biopsy forceps. Anastomosis of Aortas The donor aorta is trimmed to the minimum length required to allow anastomosis to the recipient aorta and yet avoid distortion or kinking of the left or right atrial anastomoses. An unnecessarily long donor aorta will allow the donor heart to drop back into the right pleural cavity, compressing the right lung. A short donor aorta will lift the donor heart anteriorly and superiorly, and allow for maximal expansion of the right lung posterior to the transplanted organ. Temporary inflation of the lungs at this stage will help in estimating optimal length. A sidebiting clamp is applied to the right side of the recipient ascending aorta and then is rotated anteriorly so that the anastomosis can be performed more easily. An incision equal in length to the diameter of the donor aorta is made into the aorta contained in the jaws of the clamp. The end-to-side anastomosis is made using a continuous suture of 4-0 polypropylene (see Fig 7). The cardioplegia catheter in the donor aorta is converted for use as an air vent, and the snares are released from around the caval cannulas. Anastomosis of Pulmona y Arteries In our experience the donor pulmonary artery will not adequately reach to the recipient pulmonary artery without undue tension or distortion of the other anastomoses; therefore, a conduit is inserted. Originally, a length of donor descending aorta was excised and utilized for this purpose, but more recently we have used a preclotted woven Dacron graft. The size of graft chosen will depend largely on the diameter of the donor pulmonary artery; this is usually on the order of 22 mm. (We have found a similarly sized commercially available polytetrafluorethylene graft to be less satisfactory because it does not accommodate as well to the contours of the intrathoracic anatomy. ) A longitudinal incision of suitable length is made in the main pulmonary artery of the recipient. The Dacron graft is anastomosed end-toside to the recipient pulmonary artery using continuous 5-0 polypropylene, the first stitch being placed at the distal end of the incision (see Fig 8). The graft is tailored to the correct length to bridge the gap between the two pulmonary arteries. The end-to-end anastomosis to the donor pulmonary artery is performed using continuous 5-0 polypropylene suture. To ensure a bloodless field during this procedure, it is sometimes necessary to insert a flexible sucker along the lumen of the Dacron graft into the recipient pulmonary artery; both recipient and donor pulmonary artery suckers are removed before completion of the final anastomosis. As rewarming occurs, the donor heart will either begin spontaneous coordinated contractions or lapse into vigorous ventricular fibrillation, requiring electrical defibrillation. After evacuation of air the left ventricular apical vent is removed. The recipient heart has not infrequently maintained coordinated contractions throughout the procedure; if this is the case, air

481 How to Do It: Novitzky, Cooper, and Barnard: Heterotopic Heart Transplantation corded at these sites. The left ventricle of the transplanted heart now lies anterior to the right ventricle and is therefore situated immediately under the chest wall at the sites of the V3R to V5R electrodes. DONOR RECIPIENT Fig 9. Completed operation. (See Fig 1 for abbreviations.) is removed from the left ventricle and the vent is removed. A careful inspection is made of the accessible suture lines to confirm hemostasis; the pulmonary artery and aortic anastomoses can usually be inspected satisfactorily, but it is often difficult to inspect the anterior right atrial suture line, and it is impossible to see the deeper suture lines. The venous cannula in the SVC is withdrawn into the right atrium, the IVC cannula is removed, and if the hemodynamic status of each heart is stable, cardiopulmonary bypass is discontinued and all cannulas are removed from the patient (Fig 9). The heparin is neutralized with protamine sulphate. Three drains are inserted, one into the pericardial cavity posterior to the recipient heart, a second anterior to this heart, and a third in the midaxillary line at the costodiaphragmatic angle to ensure adequate drainage of the right pleural cavity. Before closure of the chest the anesthetist is requested to ventilate both lungs fully to ensure expansion of the right lung, particularly of the lower lobe, which has been compressed by the donor heart throughout the procedure. The sternum is united with at least six wire sutures. In our experience the recipient operation can be completed in approximately 4 to 5 hours. The chest wall is tattooed with India ink injected into the dermis at points marking the electrocardiographic leads V3, V4, V5, and V3R, V4R, V5R; future electrocardiograms will be re- Comment Heterotopic heart transplantation by the technique described here connects the donor heart in parallel with the recipient heart. Preferential flow to the donor or the recipient ventricle will be directly related to the respective ventricular compliance. Ejection of blood is asynchronous, depending on the different heart rates, but does not interfere substantially with the performance of either heart [8]. Under normal circumstances, the maximal flow will be through the donor heart, since the ventricular compliance of this organ should be greater than that of the diseased recipient heart. Immediately after transplantation, however, when the donor heart is recovering from an ischemic period, or during episodes of severe acute rejection, there may be reduced compliance of the transplanted ventricles, and a greater percentage of the blood from the common atria may enter the recipient ventricles. There has been no operative or early postoperative mortality related to technical problems in the 46 patients in whom we have done transplants to date. The operation has been combined on occasion with other procedures in the recipient heart, such as resection of a left ventricular aneurysm, coronary artery bypass grafting, and mitral annuloplasty. Although heterotopic heart transplantation involves the inclusion of a prosthetic graft into a patient who subsequently will be heavily immunosuppressed, we have seen no infectious complications related to the presence of this graft. Although we believe that it is preferable to maintain perfusion of the diseased recipient myocardium throughout the operation, we have on occasion utilized a period of cardioplegic arrest and topical hypothermia of this heart without ill effects. Systemic hypothermia of 28 C is maintained largely to diminish rewarming of the donor heart by its proximity to the recipient organs during its ischemic period; if ventricular fibrillation of the recipient heart

482 The Annals of Thoracic Surgery Vol36 No 4 October 1983 occurs, topical hypothermia is used to protect the myocardium further. Neither the left nor the right atrial anastomosis must be restrictive. If the right atrial anastomosis is confined to the superior venae cavae, inadequate flow into the donor right atrium may result. Any subsequent contraction at the suture line may lead to difficulty in manipulating biopsy forceps into the donor right ventricle; in such patients left ventricular biopsy specimens must be obtained by the arterial route. The incision in each heart must be extended well down into the atrial wall. Some collapse of the right lower lobe is always present at the end of the operation, but with adequate physiotherapy this lobe expands over the course of the next few days; this has not increased the incidence of postoperative pulmonary infection in this lobe. Right lung volume remains reduced following heterotopic heart transplantation, but in no case has this been associated with symptoms of impaired ventilatory capacity. We have transplanted large adult hearts into two 14-year-old boys without problems in this respect. Donor heart excision has frequently been combined with removal of both kidneys. After the initial preparation of the donor heart, the kidneys are mobilized. While cardioplegic arrest of the heart is being induced, the kidneys are removed. Finally, excision of the cold, arrested heart is completed. We thank Ms. Jenny Bosman of the Department of Clinical Photography at Groote Schuur Hospital, who prepared the illustrations for this article. References 1. Cooper DKC: Experimental development of cardiac transplantation. Br Med J 4:174, 1968 2. Barnard CN, Losman JG: Left ventricular bypass. S Afr Med J 48:303, 1979 3. Losman JG, Barnard CN: Hemodynamic evaluation of left ventricular bypass using a homologous cardiac graft. J Thorac Cardiovasc Surg 74:695, 1977 4. Barnard CN, Barnard MS, Cooper DKC, et al: The present status of heterotopic cardiac transplantation. J Thorac Cardiovasc Surg 81:433, 1981 5. Cooper DKC, Novitzky D, Hassoulas J, Barnard CN: Heart transplantation: the South African experience. Heart Transplantation 2:151, 1982 6. Losman JG, Levine H, Campbell CD, et al: Changes in indications for heart transplantation: an additional argument for the preservation of the recipient s own heart. J Thorac Cardiovasc Surg 84:716, 1982 7. Barnard CN, Cooper DKC: Clinical transplantation of the heart: a review of 13 years personal experience. J R SOC Med 74:670, 1981 8. Beck W, Gersh BJ: Left ventricular bypass using a cardiac allograft; hemodynamic studies. Am J Cardiol37:1007, 1976