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J Thorac Cardiovasc Surg 1994;108:403-411
© 1994 Mosby, Inc.
CARDIAC AND PULMONARY REPLACEMENT |
Los Angeles, Calif.
From the Department of Surgery, Division of Cardiothoracic Surgery, University of Southern California School of Medicine, Los Angeles, Calif.
Address for reprints: Vaughn A. Starnes, MD, Department of Surgery, Division of Cardiothoracic Surgery, University of Southern California School of Medicine, 1510 San Pablo St., Suite 415, Los Angeles, CA 90033.
Abstract
Lobar transplantation represents a therapeutic option for children and some adults with severe end-stage pulmonary disease. Six patients including two neonates, three children, and one adult underwent lobar transplantation. Ages ranged from 17 days to 21 years. Transplant procedures were unilateral in the neonates and two of the children and bilateral in the child and adult who had cystic fibrosis. The donor lobes were from cadavers in the two neonates and living related donors in the children and the adult. Unilateral grafts involved use of the right upper lobe in the 12-year-old patient with bronchopulmonary dysplasia; right middle lobe with a ventricular septal defect repair in the 4-year-old patient with Eisenmenger's syndrome, left upper lobe in the 28-day-old patient with primary pulmonary hypertension, and the right upper and middle lobes in the 17-day-old patient with diaphragmatic hernia. Bilateral lobar transplantations were performed with the right lower and left lower lobes in the two patients with cystic fibrosis (aged 13 and 21 years). The two neonates underwent emergency transplantation with the use of extracorporeal membrane oxygenation as a bridge. Perioperative survival was 83%, with only the 4-year-old patient with ventricular septal defect/Eisenmenger's syndrome dying early. No airway complications were observed. The unilateral grafts received most of the blood flow as shown by perfusion scanning (range 74% to 99%). Living related donor complications included prolonged air leaks (>6 days) in two patients. In urgent situations, such as an infant requiring extracorporeal membrane oxygenation, and in the existing milieu of donor shortage, lobar transplantation (living related or cadaveric) is a surgically feasible procedure and can provide a donor source in the limited time frame of these clinical situations. Bilateral lobe transplantation may be a viable option for patients with cystic fibrosis and life-threatening respiratory decompensation. (J THORAC CARDIOVASC SURG 1994;108:403-11)
Over the past decade, many advances have been made in pulmonary transplantation which include improved surgical technique resulting in safe single and double lung transplantation, improvement in lung preservation, and improvement in the early diagnosis of pulmonary rejection. 
1-5 As a consequence of these successes, physicians now consider lung transplantation as one of the therapeutic options for patients with end-stage lung diseases. The recipient list is therefore expanding, whereas donor lung availability remains static. Therefore, many patients on the lung transplant list face the serious consequence of not receiving a lung allograft because of the lack of donors.
In an attempt to address the donor shortage, investigations have begun involving lung grafts of reduced size (lobes) for selected patients. 6,7 In initial animal experiments, the down-sized lung graft has provided adequate pulmonary functional reserve to function as an entire whole lung. 8-10 Using this experimental data, we have embarked on a clinical program using lobes from cadaveric and living related donors as the whole lung graft for selected patients.
PATIENTS AND METHODS
Indications for lobar transplantation.
The indications for lobar transplantation do not differ from those for conventional lung transplantation with whole lung allografts. 11 All patients had been previously listed for a cadaveric lung. Acute clinical deterioration without expectation of a cadaveric allograft was used as the criteria for entry into the lobar transplantation protocol. Institutional Review Board approval from Stanford University, The University of Southern California, and Childrens Hospital Los Angeles was obtained before consideration of any patient for this procedure. In those cases involving living related donors, the donors were interviewed by an independent university committee to safeguard against coercion and to ensure donor comprehension of the procedure.
Six patients underwent lobar transplantation (Table I). Two neonates were supported by extracorporeal membrane oxygenation shortly after birth until their transplantations at 17 and 28 days from donors aged 6 months and 2 years, respectively. The diagnoses in these two infants were diaphragmatic hernia and pulmonary hypertension, respectively. The lobes transplanted were the right upper and middle lobes in the 17-day-old infant and the left upper lobe in the 28-day-old infant.
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Table II contains spirometry data for five of the six living related donors. Cultures to exclude bacterial, viral, and fungal infections were performed. Serologic testing of the donor included evaluation of his or her status for hepatitis (hepatitis A, B, and C), human immunodeficiency virus, and cytomegalovirus. Determination of the cytomegalovirus status was performed to predict which patients would need prophylactic antiviral therapy. Cytomegalovirus mismatch was not used as an exclusion to transplantation.
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Surgical technique
Living related donor lobectomy.
Many factors must be considered in lobar transplantation: (1) lobar anatomy, (2) size discrepancy, (3) removal of the living related donor lung tissue, (4) removal of the recipient lung, and (5) predicting the adequacy of lung volume to be transplanted. Surgical consideration of the lobar anatomy would predict that some lobes are more amenable to removal and transplantation than others. The explantation of the right upper lobe often involves multiple arteries, necessitating the removal of the anterior wall of the donor's pulmonary artery as a Carrel patch. We have had success with this strategy when harvesting the right upper lobe, and postoperative angiography confirms that perfusion has not been compromised by this approach. After removal of the lobe, the donor's artery is reconstructed with either homograft pulmonary artery or pericardium as an onlay graft. The right middle lobe has proven to be easily removed, but it has been suggested that the right middle lobe performs more like a segment rather than a lobe with a limited microvascular bed incapable of accepting the full cardiac output in those conditions of pulmonary hypertension. In addition, the right middle lobe has inconsistent pulmonary venous drainage that may drain to the upper or lower veins or directly into the left atrium. In the removal of the right lower lobe, the middle lobe bronchus may be compromised requiring the removal of the middle lobe with the lower lobe. The left lower lobe at present seems to be the lobe most easily removed with the fewest potential complications. In part, the lobe selected for transplantation is a function of the anatomy of the individual donor, the previously performed functional parameters, and ventilation/perfusion scans.
At present, the appropriate size match between the lobe to be used and the recipient's chest cavity can only be approximated. We have used computed tomographic scans to calculate the lobe volumes in potential living related donors and determined the lung volumes in the recipient with some success. The size discrepancy issue will need further refinement as we gain experience. To date, the largest weight discrepancy was from a 112 kg father to a 20 kg daughter with the right middle lobe. In addition to volumetric considerations, the pulmonary functional capacity has to be considered. We have performed ventilation/perfusion scans and determined the ventilation and perfusion to the right versus left lung and the distribution of upper versus lower lung fields. By determining the percentage of perfusion and ventilation to a given area of the lung, we can use the spirometry data to estimate how much lung function is being transplanted.
Harvesting the donor lobe begins with dissection of the lobar vasculature. Anatomic variants are identified at this time. Fissures are then completed with stapling devices to avoid potential air leaks in the donor and the recipient after transplantation. The bronchus is isolated, with care to avoid injury to adjacent bronchi. After the dissection has been completed, heparin (300 units/kg) is administered, and the pulmonary artery, followed by the pulmonary vein, and then the bronchus are divided. This sequence avoids venous congestion, which can be injurious to the allograft. The lobe is flushed ex vivo with a cold crystalloid solution until the effluent from the pulmonary vein is clear. Ex vivo flushing is mandated because of the high potassium concentration in the preservation solution, which could potentially result in hyperkalemia in the donor. The graft is stored in cold physiologic solution with added glucose until implantation.
Recipient operation.
Because of the critical nature of the recipients' conditions, all procedures were performed with cardiopulmonary bypass. The single lung transplantations were performed through standard posterolateral thoracotomies. In the two cases of cystic fibrosis, a bilateral thoracosternotomy (clam-shell) incision was used. This procedure provides sufficient exposure for cardiac cannulation and access to the pleural spaces, including the apices and behind the hilum, which may be difficult to reach. In any patient where adhesions from chronic infections or scarring from previous incisions is anticipated, the clam-shell incision is preferred over the standard sternotomy. Before administration of heparin for cardiopulmonary bypass, preliminary dissection of the hilar areas and lysis of adhesions with cautery are carried out to minimize bleeding. After this preliminary dissection has been completed and the allograft is ready, cardiopulmonary bypass is initiated and the recipient pneumonectomy is begun. The division of the pulmonary artery and veins in the recipient is performed as distally in the parenchyma of the lung as possible (Fig. 2). This positioning provides the needed vascular tissue which is sometimes required to perform the allograft implantation. The bronchus is divided at the level of the takeoff of the upper lobe with the use of a stapling device.
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12 with the exception of the use of nonabsorbable sutures. Limiting the amount of peribronchial dissection and mild telescoping of donor into recipient bronchus has provided excellent healing of the airway anastomosis without the need for an omental wrap. The anastomosis of the bronchus (Fig. 3) brings the donor lobar vein in closest approximation to the superior pulmonary vein of the recipient. The venous anastomosis is then performed in a running fashion with the lobar vein of the donor anastomosed to the superior pulmonary vein of the recipient (Fig. 4). We have found it difficult to perform a direct anastomosis to the left atrium in the recipient because of the short vein length of the donor graft, which emphasizes the need to leave adequate length on the recipient's pulmonary veins at the time of the pneumonectomy. The pulmonary artery anastomosis (Fig. 5) is performed end to end with 5-0 polypropylene suture. At the completion of the implantation, transesophageal echocardiography and bronchoscopy are performed to exclude any technical complications.
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Monitoring of rejection has included the usual clinical parameters of hypoxemia, tachypnea, and decreasing pulmonary function tests. The chest radiogram showed the typical hilar distribution of infiltrates associated with pulmonary rejection seen in conventional lung transplants. Transbronchial biopsies have been successfully performed in lobes from adults without difficulty. Rejection episodes have been managed with pulse steroids after infections have been excluded on bronchoalveolar lavage.
RESULTS
Our experience consists of lobar transplantations in six patients varying in age from 17 days to 21 years. The two neonates received allografts from cadaveric donors. Four patients received lobes from their parents. A 12-year-old child received the right upper lobe of her mother for the diagnosis of bronchopulmonary dysplasia. A 4-year-old child with Eisenmenger's syndrome received the right middle lobe from her father and underwent repair. This case was the only perioperative death and seemed to be attributable to inadequate microvasculature in the allograft with the persistence of pulmonary hypertension after discontinuance of cardiopulmonary bypass. The graft developed massive pulmonary edema approximately 4 hours after transplantation.
Two patients with cystic fibrosis received bilateral lobar transplants, with each parent donating a lobe. In each case, the mother and father were in the same ABO blood group as the recipient. The mothers on each occasion donated their right lower lobe, and the fathers donated their left lower lobes.
Rejection.
Episodes of acute rejection as diagnosed by chest radiography, clinical findings, and transbronchial biopsy were responsive to pulse steroid therapy. One neonate had a rejection episode at 10 days that responded to therapy. In the surviving recipients of living related donor transplants, only mild rejection was noted in one patient, and it responded to an increase in maintenance immunosuppression. One adolescent stopped her immunosuppressive medications on several occasions, and eventually graft dysfunction resulted. This patient is alive but requires home oxygen therapy.
Perfusion distribution.
In cases involving a unilateral transplant, the lobe received the majority of pulmonary perfusion (Table III). The 17-day-, 28-day-, and 12-year-old transplant recipients had 85%, 99%, and 74% perfusion to their transplanted lobes on perfusion scans, which showed the ability of a lobe to accommodate the entire (99%) cardiac output of the recipient if needed. In the two patients with cystic fibrosis with bilateral lobar transplants, the perfusion was balanced between right and left with equal distribution of ventilation.
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Table III). One late death occurred at 10 months as a result of respiratory syncytial virus pneumonia in the infant who received a left upper lobe. The 17-day-old infant who underwent transplantation for diaphragmatic hernia continued to do well 2.5 years after transplantation. The first double lobar transplant was without any restrictions 9 months after transplantation, and the patient's activity level was excellent. The measured forced expiratory volume in 1 second is 1.91 L/sec, which is 65% predicted, and a forced vital capacity of 2.98 L, which is 82% predicted. The postoperative chest radiograms have remained clear with complete filling of the thoracic cavities (Fig. 6, A and B). The second double lobar transplant at 5 months after the operation had a forced expiratory volume in 1 second of 1.56 L/sec, which is 69% predicted, and a forced vital capacity of 1.74 L, which is 70% predicted. Of the eight bronchial anastomoses performed in six patients, no omental wraps were performed and no airway complications were seen.
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DISCUSSION
Lobar transplantation, like some of the patients in this report, is in its infancy. The preliminary results support the continued investigation of this procedure for patients with end-stage lung disease and acute deterioration. Many questions remain to be answered: Which is the most appropriate lobe to transplant? Does the mature lobe in a child grow? How is the amount of lung tissue to be transplanted best determined? Patients with Eisenmenger's syndrome and primary pulmonary hypertension can be expected to shunt the majority of the cardiac output through the transplanted lobe. Careful selection of the donor lobe must include the consideration of this posttransplantation shunt phenomenon. The lobe or lobes chosen for transplantation must be capable of handling the majority of the cardiac output, which may exclude some lobes from consideration (right middle lobe). In the one perioperative death, the right middle lobe was used in a 4-year-old patient with Eisenmenger's syndrome, and postoperative pulmonary hypertension, pulmonary edema, and death resulted. This outcome was probably related to inadequate pulmonary microvasculature in the middle lobe.
At present, lobar transplantation seems to be best suited for children and small adults with a weight range from 20 to 50 kg. This weight range has permitted anatomic lobes to be transplanted without the need to tailor the graft further at the time of transplantation. As the size discrepancy increases, the number of functioning alveolar units and the microvascular bed of the graft becomes a matter of concern. With an increasing donor-recipient ratio, smaller lobar units are considered for volumetric reasons. However, our concern is that they may not be best suited physiologically because of this inadequate pulmonary microvasculature. In our anecdotal experience of one patient with a large weight discrepancy (more than sixfold), the transplanted graft seemed to have inadequate pulmonary microvasculature.
Although we have on occasion transplanted each of the pulmonary lobes, the right and left lower lobes seem most suitable for the recipient's right and left sides, respectively. Transplantation of the right upper lobe necessitated removal of the pulmonary arteries as a Carrel patch, with reconstruction of both the donor pulmonary artery and the arteries of the transplanted lobe. The complexity of this procedure, as well as the variability of the pulmonary arterial anatomy to the right upper and middle lobes, has discouraged us from using the right upper lobe on a regular basis.
This experience documents the technical feasibility of lobar transplantation. However, a major issue is the physiologic behavior of the mature lobe transplanted into a child. Preliminary animal experience suggests that the number of functioning alveoli does not increase but that hypertrophy may occur. 13 If the air space enlargement is in proportion to increases in the microvasculature, the functioning unit should be preserved with a good physiologic outcome for the recipient. If however, emphysematous changes occur, then this outcome would be unacceptable. Despite these uncertainties, this operation needs to be further investigated because of the certainty of death in these patients with end-stage disease where acute deterioration is occurring without an available donor.
Appendix: DISCUSSION
Dr. Harold C. Urschel, Jr. (Dallas, Tex.).
Why use two related donors (mother and father) on one patient. Why not use one lobe from one donor and perform a pneumonectomy on the other side? This has several advantages: (1) it provides adequate ventilation, (2) it uses up only one donor and doubles the supply, (3) there is less chance for rejection, and (4) it is a shorter and simpler procedure.
Second, I would agree that the ethical and psychologic ramification of related donors should be addressed carefully. However, regarding transplantation and use of related donors, it is certainly not as new as was intimated in the discussion. The first successful renal transplantation was between identical twins (I was present when the kidney was carried from table to table). The wife of an honorary member of the organization gave a renal transplant to her daughter many years ago. Even crosscirculation for a pair of heart defects with one of the parents as the pump-oxygenator has been successfully performed.
This epic paper honestly presented will open many opportunities in pulmonary transplantation.
Dr. Starnes.
To implant only a lobe on one side and perform a pneumonectomy on the other side in the recipient with cystic fibrosis would be high risk. We believe a single lobe would not provide adequate pulmonary reserve. In addition, in patients with cystic fibrosis, the risk of a postpneumonectomy closed space infection would be high.
Paul F Waters (Los Angeles, Calif).
Dr. Starnes and his group, in this preliminary report, have demonstrated that it is possible to transplant units smaller than a whole lung and achieve success in short-term follow-up. I congratulate him for this accomplishment. Although a small number of patients are included, there are actually a number of subgroups that warrant separate discussion.
In the pediatric group, where lobes from either living related or cadaveric adults are used to substitute as a whole lung, there is a real question of what the long-term outcome will be. We know that the adult lung has no capacity to increase in size by regeneration; therefore, what will happen when the child grows and the lobe does not is an unknown factor. It is conceivable that it will become emphysematous or that scoliosis may occur as a compensatory mechanism. In any case, it would seem reasonable to offer this as a bridge procedure at least in the desperately ill child or infant recipient where no child donor appears to be forthcoming. Dr. Starnes, do you have any information from the experimental laboratory on the long-term outcome of adult lobes when implanted into young animals as they mature?
In the adult group, confined to cystic fibrosis in this report, we are told of two cases where both parents donated one lower lobe as a whole lung substitute for double lung replacement in two recipients. One patient is in her fifth postoperative month and appears to be doing well, whereas the second patient is apparently recovering in hospital 1 month after the transplantation. In this group, my question is basically one of the difficult ethical situation we as transplanters find ourselves in, given the extreme shortage of donor organs. The currently accepted 1-year survival for lung transplantation in cystic fibrosis is in the 60% to 70% range, and, although not completely analogous, the Lung Cancer Study Group data show a mortality of about 1% for pulmonary lobectomy. Although removing normal lobes probably carries a lower figure, the mortality is almost certainly not 0% and will be higher if a whole lung is removed (which I suppose is the next logical development). We therefore must accept that sooner or later a living related donor in this situation will die of the consequences of providing an organ for a loved one who has, at best, a 70% 1-year posttransplantation survival. Furthermore, institutional review committees not withstanding, it seems to me that it is going to be difficult for a parent or close relative to say no when approached by a transplant team to request their donation of a lung or lobe. It is not fair to compare this with other organs, such as the kidney, where living-related donation is established and appropriate. If the kidney transplantation is unsuccessful, the recipient does not usually die, which is often the case in lung transplantation. I am not suggesting that living related donor lung donation is not a possibility but urge that the complete ethical and moral implications be studied carefully and every possible step to avoid coercion be taken.
Finally, Dr. Starnes, in your illustration of the technique of donor left lower lobectomy, it was not clear how the lingular branches of the pulmonary artery were handled. Were they sacrificed or preserved in some way?
Dr. Starnes.
Regarding the issue of growth in the pediatric population, long-term follow-up is clearly needed. To date, the 12-year-old patient has had increased lung function despite somatic growth with no physical handicaps. Animal work in a porcine model of a mature lobe to an immature recipient is currently in progress. The operation may well be most applicable in children at least 15 to 20 kg and above as opposed to the neonatal population.
On the basis of our total up-to-date experience with bilateral lobar transplantation in 11 patients with cystic fibrosis, we have had 10 survivors with excellent functional status and we have had no long-term morbidity in any of the donors. If the lingular artery in the donor is a single large vessel, we have reimplanted it into the left pulmonary artery. If there are multiple small arteries to the lingula, then the branch has been ligated.
Footnotes
Read at the Nineteenth Annual Meeting of The Western Thoracic Surgical Association, Carlsbad, Calif., June 23-26, 1993. 
References
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R. J. Battafarano, R. C. Anderson, B. F. Meyers, T. J. Guthrie, D. Schuller, J. D. Cooper, and G. A. Patterson Perioperative complications after living donor lobectomy J. Thorac. Cardiovasc. Surg., November 1, 2000; 120(5): 909 - 915. [Abstract] [Full Text] [PDF]
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