Ann Thorac Surg 1997;64:307-312
© 1997 The Society of Thoracic Surgeons
Original Articles: General Thoracic
Use of Over-Sized Mature Pulmonary Lower Lobe Grafts Results in Superior Pulmonary Function
Oliver A. R. Binns, MD,
Nuno F. DeLima, MD,
Scott A. Buchanan, MD,
Robert C. King, MD,
Jeffery T. Cope, MD,
James D. Maliszewskyj, BS,
Curtis G. Tribble, MD,
Irving L. Kron, MD
Division of Thoracic and Cardiovascular Surgery, Department of Surgery, University of Virginia Health Sciences Center, Charlottesville, Virginia
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Abstract
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Background. Mature lobar transplantation will increase the pediatric donor organ pool; however, issues regarding size discrepancy between donor grafts and recipient lungs remain unresolved. We hypothesized that an over-sized mature pulmonary lobar allograft implanted into an immature recipient would provide adequate long-term pulmonary function versus a size-matched mature lobar graft or an immature whole lung.
Methods. We investigated our hypothesis in a porcine orthotopic left lung transplant model in which 19 immature animals made up one control and three recipient groups. Group I underwent sham left thoracotomy (control, n = 4). Group II received age- and size-matched immature whole left lung transplant (n = 6). Group III received mature size-matched left upper lobe transplants (n = 4). Group IV received mature over-sized left lower lobe transplants (n = 5). Twelve weeks after implantation, data were collected after the native right lung was excluded.
Results. Graft weight was significantly elevated in group IV as compared with the explanted lung (72.4 ± 6.8 versus 38.3 ± 4.5 g; p = 0.003). Pulmonary artery pressure and pulmonary vascular resistance were significantly elevated in group III as compared with the over-sized mature lower lobe transplants (51.8 ± 2.2 versus 40.4 ± 2.5 mm Hg [p < 0.0001] and 1,605.9 ± 117.5 versus 857.6 ± 133.6 dynes · s · cm-5 [p < 0.0005], respectively). A trend toward decreased oxygenation was identified in group II.
Conclusions. Over-sized mature lobar grafts provide improved hemodynamics as compared with size-matched grafts. Mature left lower lobe grafts are superior to size-matched upper lobe grafts in this model, probably as a result of an augmented vascular bed.
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Introduction
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Pulmonary transplantation has become a successful therapeutic option for patients with end-stage pulmonary disease. With this success, and its increasing application for a diverse group of lung diseases, the critical donor shortage has become even more evident. Approximately 25% of patients on recipient waiting lists will die of their underlying pulmonary disease while awaiting identification of a suitable donor [1]. This limitation to lung transplantation is especially pertinent to the pediatric population, where organ availability is further limited by size discrepancies between the potential recipient and donor.
Lobar transplantation from living-related and cadaveric donors has been used to meet this increasing demand for donor organs [2, 3]; however, the issue of acceptable size discrepancy between donor and recipient organs has yet to be resolved [4, 5]. As size mismatch may limit effective organ utilization and lead to refusal of organ acceptance [1], the use of over-sized grafts could potentially expand the donor pool. Previous work in our laboratory demonstrated that transplantation of mature lung tissue may be functionally superior to the use of immature allografts in developing recipients [6]. In an effort to further define acceptable size disparities using mature lobar allografts we hypothesized that an over-sized mature pulmonary lobar allograft implanted into an immature recipient would provide adequate long-term pulmonary function as compared with a size-matched mature lobar graft or an immature whole lung. We used a porcine orthotopic left lung transplant model to investigate our hypothesis. Major histocompatibility complex-matched animals were used to minimize the confounding effects of chronic rejection in these long-term studies [7].
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Material and Methods
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Experimental Protocol
Nineteen immature swine made up one control and three recipient study groups. Nine mature and 6 immature swine (major histocompatibility complex matched with recipients) served as lung donors. Immature recipients were 12 weeks of age and less than 10 kg in total body weight. Mature donors were at least 1 year of age and averaged 42.2 ± 6.4 kg in total body weight. Immature donors were age- and size-matched with the recipient, averaging 7.9 ± 0.5 kg in total body weight. Group I (control) underwent sham left thoracotomy (n = 4). Group II (IWL TXP) received age and size-matched immature whole left lung transplants (n = 6). Group III (MUL TXP) received mature size-matched left upper lobe transplants (n = 4). Group IV (MLL TXP) received mature over-sized left lower lobe transplants (n = 5). All lungs were flushed with cold Euro-Collins solution before preparation of the graft for implantation.
Harvest Procedure
We used the following experimental model previously described by our laboratory [6, 8]. Nine adult major histocompatibility complex-matched Hanford miniature swine served as mature lobar donors. Six immature age-, size-, and major histocompatibility complex-matched swine served as immature whole lung donors. Anesthesia was induced with intramuscular xylazine (1 mg/kg) and telazol (6 mg/kg). Atropine (0.01 mg/kg) was used to facilitate endotracheal intubation. Ventilation was instituted with room air at a rate of 16 breaths/minute using a volume ventilator (Harvard Apparatus, Natick, MA) with a tidal volume of 15 mL/kg. Animals were paralyzed with metocurine (0.2 mg/kg). Anesthesia was maintained with 2.0% inhalational halothane.
A left posterolateral thoracotomy was performed, entering the chest through the fifth interspace. The hemiazygos vein was ligated and divided, facilitating exposure to the left hilum. The inferior pulmonary ligament was transected and the pulmonary vessels were isolated. The incomplete fissure between the left upper lobe and lower lobe was sharply divided in the mature lobar donors. Care was taken to carry out the dissection on the side of the nonused lobe to avoid air leaks in the recipient. The branches of the pulmonary artery were isolated. Each animal was then anticoagulated with intravenous heparin sodium (200 U/kg). The main pulmonary artery (PA) was clamped and a 16-gauge catheter was inserted into the vessel. A left atriotomy was then performed to vent the heart. One liter of Euro-Collins solution at 4°C was infused into the PA from a height of 30 cm. Topical cooling was achieved with cold saline slush. Room air ventilation was continued during the Euro-Collins flush. The lung was then excised and prepared for implantation.
Mature lobar grafts were prepared ex vivo. Lower lobe grafts were prepared by an upper lobectomy. The donor lower lobe pulmonary artery and bronchus were then transected. The pulmonary artery was transected just distal to the lingular artery, still allowing enough length for performance of the anastomosis without obstructing the artery to the superior segment. In animals where the lingular artery came off distal it was ligated and the anastomosis was performed proximal to the take-off. The bronchus was divided as close to the take-off of the sixth segmental bronchus as possible, still allowing enough length for the anastomosis to be accomplished. Upper lobe grafts were prepared by performing a left lower lobectomy. The upper lobe bronchus was prepared with a cuff of main bronchus to allow for size mismatching. The venous anastomoses were accomplished with a left atrial cuff. The upper and lower lobe veins were identified as they entered the atrium and appropriately ligated, care being taken not to encroach upon the upper lobe venous ostium for upper lobe grafts or the lower lobe venous ostium for lower lobe grafts.
Recipient Pneumonectomy and Implantation
Fifteen immature major histocompatibility complex-matched swine served as left lung recipients. Four immature animals underwent a sham left thoracotomy. Recipients received cyclosporine (18 mg/kg) (Sandimmune; Sandoz Pharmaceuticals Corp, East Hanover, NJ) and aspirin (325 mg) 1 day before transplantation. On the day of the operation, anesthesia was induced similarly to donors and followed by intubation. Ventilation was instituted with 100% oxygen. Azathioprine (1 mg/kg) and methylprednisolone (500 mg) were administered intravenously along with cefazolin (250 mg) before the skin incision. Anesthesia was maintained with 1.5% inhalational isoflurane. Through a left posterolateral thoracotomy, the left lung was mobilized and the hilum dissected as in the donor pigs. Dissection around the recipient bronchus was minimized. In addition, care was taken to avoid injury to the phrenic nerve. The recipient was then anticoagulated with intravenous heparin sodium (200 U/kg), the pulmonary artery was clamped, and the pulmonary veins and artery were ligated and divided. The left main bronchus was then clamped, and the left lung was excised.
Implantation commenced with the bronchial anastomosis, followed by the pulmonary arterial and left atrial anastomoses. All anastomoses were carried out using absorbable suture to allow for growth. The bronchial anastomosis was carried out using a continuous 5-0 monofilament polydiaxone suture (PDS II; Ethicon, Inc, Somerville, NJ). The donor bronchus was intussuscepted into the recipient bronchus approximately 4 to 6 mm to achieve a telescoping anastomosis. In animals receiving mature lower lobe grafts, the recipient bronchus was telescoped into the donor bronchus. The large diameter of the mature lower lobe donor bronchus as compared with the immature recipient's main bronchus necessitated this difference in technique. The bronchial clamp was removed upon completion of the airway anastomosis. The transplanted graft was ventilated, and the anastomosis was examined under saline solution for evidence of air leak. The graft was ventilated with 100% oxygen until completion of the remaining anastomoses. The pulmonary arterial anastomosis was then completed using a continuous 6-0 polydioxanone suture (PDS II). The left atrial cuff anastomosis was carried out with a continuous 5-0 polydioxanone suture (PDS II). At this time, the animal received a second dose of heparin sodium (100 U/kg), and the vascular clamps were removed. The end of the ischemic interval was noted. Intercostal nerve blocks were performed using 0.25% bupivicaine HCl (Sensorcaine; Astra Pharmaceutical Products, Westborough, MA). A 16F chest tube was inserted through the seventh intercostal space. The chest wall was closed in layers, and the chest tube was connected to a water seal chest drainage system (Atrium Medical Corp, Hudson, NH) using 20 cm of water suction. All animals were extubated within 1 hour postoperatively. Chest tubes were removed by postoperative day 2, and the animals were fed on postoperative day 1.
Immunosuppression consisted of cyclosporine (18 mg · kg-1 · day-1), azathioprine (1 mg · kg-1 · day-1), and corticosteroids. Cyclosporine administration was continued for 7 days. Azathioprine administration was continued for the full 3-month growth period. Methylprednisolone (500 mg/day) was administered daily for 7 days and then switched to maintenance prednisone (2 mg/kg orally per day), which was continued for 3 months. Additionally, each animal received a daily 325-mg aspirin tablet and Bactrim DS (trimethoprim and sulfamethoxazole; Roche Laboratories, Nutley, NJ) one tablet orally twice per day. Administration of cefazolin (250 mg daily) was continued for 7 days postoperatively. Chest radiographs were obtained 6 weeks after transplantation.
All animals received humane care in accordance with the "Guide for the Care and Use of Laboratory Animals" (National Institutes of Health publication 85-23, revised 1985.) The protocol was reviewed and approved by the Animal Review Committee of the University of Virginia.
Data Collection
After 3 months of growth and development, each animal was anesthetized with intramuscular xylazine and telazol. Atropine was administered, and the animals were intubated. A second chest radiograph was obtained to document aeration of the transplanted lung. A tracheostomy was then performed, through which a no. 9 cuffed endotracheal tube was inserted. The animal was ventilated with room air. The right carotid artery and internal jugular vein were dissected, and a 16-gauge catheter was placed in the carotid artery for pressure measurements and blood gas analysis. A large-bore introducer was placed in the right internal jugular vein for intravenous access. A balloon-tipped PA catheter was floated into the PA with placement guided by wave forms. Carotid artery, central venous, and pulmonary artery pressures were continuously measured with a multichannel recorder (Hewlett Packard 78353B, Santa Clara, CA). Flexible bronchoscopy was performed using a pediatric bronchoscope with an outer diameter of 3.5 mm. The bronchial anastomosis was examined for evidence of narrowing or technical complications before collection of functional data.
PULMONARY AIRWAY MECHANICS.
Dynamic airway data were recorded during double-lung ventilation and again after exclusion of the native right lung. Air flow was measured using a Fleisch no. 0 pneumotachometer, which was connected to a differential transducer and an analog-to-digital converter (AII Devices, San Raphael, CA). An Apple II microcomputer (model A2M2010) was used to collect data. Airway pressure was simultaneously recorded using a pressure transducer (model MP45-26-871; Validyne Engineering Corp, Northridge, CA). Pressure-volume loops were constructed from single tidal inflations by hand editing the three points of zero flow (beginning inspiration, peak inspiration, and end expiration) with a manual cursor and editor. Dynamic compliance was calculated as the slope of the line of best fit (least squares method) through the origin and apex of this pressure-volume relationship. Pressure-volume loops for the transplanted lung alone were then constructed after occlusion of the native right lung airways using a 6F Fogarty balloon catheter (model CV1048; Baxter Healthcare Corp, Santa Ana, CA). The catheter was positioned and inflated in the right main bronchus under direct vision with the aid of a bronchoscope. To occlude the right eparterial bronchus present in swine, we performed proximal left main bronchial intubation. The endotracheal tube cuff was then inflated to occlude the airway to the right upper lobe.
PULMONARY HEMODYNAMICS.
Baseline hemodynamic data (pulmonary artery pressure, cardiac output, systemic blood pressure, and pulmonary capillary wedge pressure) were obtained at the initiation of the study. After completion of the dynamic airway measurements, a median sternotomy was performed. Accurate placement of the PA catheter into the pulmonary artery was confirmed by palpation. Mean PA pressure (PAP) and pulmonary capillary wedge pressure were recorded at end expiration. Cardiac output was measured in triplicate by the thermodilution technique using the thermistor-tipped Swan-Ganz catheter. Double-lung pulmonary vascular resistance (PVR) was calculated by the equation PVR = (mean PAP - pulmonary capillary wedge pressure)/cardiac output x 80. The PA catheter was then pulled back into the proximal PA, and the right hilum was totally occluded with a large vascular clamp. Care was taken to assure complete cessation of blood flow and ventilation to the native lung. The animal was allowed to stabilize for 15 minutes. Repeat measurements of mean PAP, pulmonary capillary wedge pressure, and cardiac output were recorded while the animal was totally dependent on the transplanted lung. The PVR of the transplanted lung was calculated as above.
STUDIES OF GAS EXCHANGE.
Blood gas measurements were obtained under conditions of double-lung ventilation and again during single-lung ventilation 15 minutes after right hilar clamping. Arterial blood specimens were collected using room air ventilation and with an inspired oxygen fraction of 0.70. Double-lung ventilation was carried out with a tidal volume of 15 mL/kg. Ventilation of the transplant lung after right hilar clamping was carried out with a tidal volume of 12 mL/kg. Blood gas samples were run on a Corning 178 pH/Blood Gas Monitor (CIBA Corning Diagnostics, Medfield, MA). At the completion of the study, the animal was euthanized with a lethal dose of sodium pentobarbital, and the transplanted lung was excised.
Statistical Analysis
Measurements are reported as the mean ± the standard error of the mean. Analysis of variance was used to determine if significant differences existed between groups. A p value of 0.05 or less was used to indicate a significant difference between measurements.
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Results
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Size Disparity
Donor-to-recipient total body weight ratios were as follows: the IWL TXP group had a ratio of 0.87, the MUL TXP group had a ratio of 4.35, and the MLL TXP group had a ratio of 4.18. The mean explanted lung weights at the time of implantation were 41.5 ± 2.0 g (IWL TXP), 42.2 ± 5.6 g (MUL TXP), and 38.3 ± 4.5 g (MLL TXP). The mean graft weights at the time of implantation were 34.6 ± 1.5 g (IWL TXP), 32.8 ± 1.3 g (MUL TXP), and 72.4 ± 6.8 g (MLL TXP). This resulted in a significant increase in graft weight versus explant weight in the MLL TXP group (p = 0.003) (Fig 1
). There were no significant differences in graft weight versus explant weight in either the MUL TXP or IWL TXP groups. Average graft-to-explant weight ratios were as follows: 0.83 (IWL TXP), 0.78 (MUL TXP), and 1.89 (MLL TXP).
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Fig 1. . Comparison between explanted lung weight ( Explant Wt) and graft weight (Graft Wt) at the time of implantation. Mature lower lobe grafts (MLL TXP) were significantly larger than the recipient's explanted lung. (IWL TXP = immature whole left lung transplant; MUL TXP = mature left upper lobe transplant; NS = not significant.)
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Technical Results
The mean implantation times were as follows and demonstrate a trend toward increased ischemia for the mature lower lobe transplants: IWL TXP (90.3 ± 3.9 minutes) and MUL TXP (101.0 ± 6.1 minutes) versus MLL TXP (110.2 ± 7.4 minutes) (p = 0.074). There were no prolonged air leaks, and all chest tubes were removed by postoperative day 2. All animals demonstrated normal aeration of the transplanted lungs radiographically (Fig 2). There were no airway complications, although granuloma formation at the anastomotic site in 1 immature whole lung recipient resulted in a slight narrowing of approximately 20% that was functionally insignificant. One mature lower lobe recipient also had an insignificant narrowing due to a small cartilaginous shelf at the anastomosis. In all animals the pulmonary arterial and left atrial anastomoses were patent without thrombosis.
Functional Results
The following parameters of pulmonary function were determined after exclusion of the native right lung, thereby reflecting only the transplanted graft's function: PAP, PVR, pulmonary compliance, and oxygenation. All animals were able to survive exclusion of the native right lung, and elevations in PAP and PVR occurred in all lungs after clamping of the native right hilum. A significant elevation in PAP was identified in the MUL TXP group (Table 1). Similarly, elevation in the PVR was identified when comparing the MUL TXP group with the controls and other experimental recipients (Fig 3). No differences in pulmonary compliance between the groups existed; however, the IWL TXP group demonstrated the lowest mean (Fig 4). Oxygenation was equivalent between groups on room air; however, with an inspired oxygen fraction of 0.70 a trend toward worsening function with the use of immature whole lungs was demonstrated (Table 1; Fig 5).
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Fig 3. . Pulmonary vascular resistance of the transplanted lung after the native right lung was excluded. The mature upper lobe group ( MUL TXP) demonstrates a significant elevation in pulmonary vascular resistance. (IWL TXP = immature whole left lung transplant; MLL TXP = mature left lower lobe transplant.)
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Fig 4. . Lung compliance of the transplanted lung. No significant differences were demonstrated between groups. ( IWL TXP = immature whole left lung transplant; MLL TXP = mature left lower lobe transplant; MUL TXP = mature left upper lobe transplant.)
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Fig 5. . Oxygenation by the transplanted lung. A trend toward decreased oxygenation ( p = 0.06 versus mature left upper lobe grafts [MUL TXP]) was seen with the use of immature whole lung grafts (IWL TXP). (MLL TXP = mature left lower lobe transplant.)
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Comment
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Since the first human lung transplantation performed by Hardy and associates in 1963 [9], pulmonary transplantation has become an accepted therapeutic option for adult patients with end-stage lung disease. Along with this success has come the widespread application of lung transplantation. Similarly, lung transplantation has been increasing applied in the pediatric population to treat a diverse group of primary pulmonary pathologies and secondary pulmonary hypertension due to congenital heart disease [10]. However, as with many other organs, donor lung availability has limited the number of transplant procedures being performed.
This critical shortage of donor lungs poses an even greater problem in pediatric transplantation as appropriate size matching for small recipients places further restrictions on the number of available organs. Lillehei and associates [4] reported a 32% mortality in 22 patients who were awaiting identification of a suitable donor. In light of this shortage of available organs, alternative reduced-size lung transplants have been proposed and used in the setting of acute clinical deterioration [5]. As with transplantation of whole lungs, size-matching of the lobar graft to the recipient's thoracic cavity and functional needs remains a critical issue. Selection of the lobar graft has been based on computed tomographic volume calculations and perfusion scans; however, the acceptable minimum volume of lung tissue to allow recipient survival has not been determined [11]. Similarly, the acceptable upper limit of lung tissue that a recipient can accommodate also remains unknown. The successful use of over-sized grafts could potentially provide increased organ allocation to the pediatric population and may provide additional functional benefits.
Staple pneumoreduction has been proposed as a reliable method of transplanting over-sized lungs [1, 12]. In the pediatric population a certain degree of size discrepancy is virtually always present; however, the acceptable limits have yet to be defined. Staple pneumoreduction provides a method of dealing with unexpected inordinate size mismatches, but it may be unnecessary for tolerable mismatches and functionally detrimental. In our model we have demonstrated the feasibility of successfully transplanting over-sized grafts with an average implant-to-explant ratio of 1.89 (range, 1.46 to 2.57). All recipients of over-sized grafts in our experiment survived the 3-month postoperative period and their transplants demonstrated excellent function. Over-sized grafts should not preclude transplantation, and the limits of size discrepancy requiring pneumoreduction remain to be determined.
In addition to differences in physical volumes between the graft and the recipient's chest cavity, size discrepancy between the explanted lung and graft presents changes in the available pulmonary vascular bed. Such alterations may become critical in situations where much of the cardiac output is diverted through the newly implanted lung, as is the case in single-lung transplantation when a degree of pulmonary hypertension is present. Over-sized grafts could potentially accommodate this increased blood flow after implantation more effectively than grafts with limited vascular reserve. Conversely, small grafts have been unable to compensate in this situation. In 1 of their first 3 patients undergoing lobar transplantation, Starnes and colleagues [2] reported the development of immediate postoperative edema in a child receiving a living-related right middle lobar transplant. In this patient with Eisenmenger's syndrome, the elevated pulmonary artery pressure failed to decrease in the postoperative period, leading to reperfusion pulmonary edema and her demise [2]. In a review of 10 pediatric lung recipients, Lillehei and coworkers [4] attributed two of three hospital deaths to right ventricular failure secondary to elevated pulmonary artery pressures associated with the use of small donor allografts.
Our results support these findings and suggest that an over-sized graft provides superior hemodynamics and may be especially advantageous in settings where it is anticipated that a majority of the cardiac output will be shunted through the transplanted lung. The over-sized mature lower lobe recipient group demonstrated the lowest PVR of all the transplants. An unacceptable increase in PAP and PVR was demonstrated with the use of size-matched mature upper lobe grafts, suggesting that the limited vascular bed was unable to accommodate the increased blood flow. It is possible that the hemodynamic advantages of the lower lobe grafts are attributable to anatomic differences in vascular capacitance as compared with the upper lobe, and not related to the overall size of the graft. Further studies using oversized upper lobe grafts are needed to resolve this issue. Survival of these recipients until the time of final study can be attributed to the presence of a healthy native right lung in this experimental model, although this is merely speculative without the documentation of perfusion scans. Despite these hemodynamic changes after exclusion of the native right lung, oxygenation in the mature upper lobe group was not affected. However, this arterial blood gas measurement was obtained only 15 minutes after the entire cardiac output was shunted through the graft, perhaps too short an interval to manifest the effects of ensuing congestive heart failure. In any case, these elevations in PVR would cause unacceptable long-term detriment to the right ventricle of such recipients.
Despite these apparent functional advantages, the use of over-sized grafts is also potentially problematic. Chest closure can be difficult, mediastinal shifting may occur with hemodynamic instability, and an increase in atelectasis could lead to an increased incidence of postoperative pneumonia [1]. With the use of widely disparate lungs, Lillehei and coworkers [4] reported difficulties with chest closure requiring linear stapling for pneumoreduction, allograft lobectomy, and in 1 case the use of a silicone sheet for temporary chest closure. We had no technical difficulties in closing the chest even with our largest graft-to-explant ratio of 2.57. It is likely that these over-sized grafts were subject to atelectasis; however, early postoperative chest radiographs were not obtained to document this. We did not see an increased incidence of pneumonia in these recipients, and in fact none of the recipients demonstrated any clinical manifestations of pneumonitis. Our model of single-lung transplantation may have allowed for mediastinal shifting and an altered diaphragmatic contour, thereby more readily accommodating these large grafts.
As we are confronted with a limited number of available lung grafts and a high mortality rate for recipients awaiting transplants, we must continue to investigate techniques that will allow maximum organ utilization while maintaining excellent functional results. Our results demonstrate that either mature lobar grafts or immature whole lungs can function adequately in developing recipients. The use of over-sized mature lower lobar grafts provided improved hemodynamic function as compared with size-matched grafts and did not result in an increased rate of complications in this long-term survival porcine model of orthotopic left lung transplantation. Over-sized lobar grafts may be preferential to size-matched grafts for single-lung transplantation, especially in the setting of pulmonary hypertension.
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Acknowledgments
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This work was supported by the National Institutes of Health under R01 grant HL 48242 and National Research Service Award fellowship F32HL09115-01A1. Additional support came from CNPq-Conselho Nacional de Desenvolvimento Cientifico e Tecnologico, Brazil. The technical advice of Anthony J. Herring is acknowledged.
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Footnotes
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Presented at the Poster Session of the Thirty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Feb 3–5, 1997.
Address reprint requests to Dr Kron, Division of Thoracic and Cardiovascular Surgery, Department of Surgery, University of Virginia Health Sciences Center, Box 310, Charlottesville, VA 22908.
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References
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- Starnes VA, Lewiston NJ, Luikart H, Theodore J, Stinson EB, Shumway NE. Current trends in lung transplantation: lobar transplantation and expanded use of single lungs. J Thorac Cardiovasc Surg 1992;104:1060–6.[Abstract]
- Bisson A, Bonnette P, El Kadi NB, Leroy M, Colchen A. Bilateral pulmonary lobe transplantation: left lower and right middle and lower lobes. Ann Thorac Surg 1994;57:219–21.[Abstract]
- Lillehei CW, Shamberger RC, Mayer JE, et al. Size disparity in pediatric lung transplantation. J Pediatr Surg 1994;29:1152–6.[Medline]
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- Kern JA, Tribble CG, Chan BK, Flanagan TL, Kron IL. Reduced-size porcine lung transplantation: long-term studies of pulmonary vascular resistance. Ann Thorac Surg 1992;53:583–9.[Abstract]
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- Kern JA, Kron IL. Reduced-size lung transplantation. Austin: R.G. Landes Co, 1993:42–54.
- Hardy JD, Webb WR, Dalton ML, Walker GR. Lung homotransplantation in man. Report of the initial case. JAMA 1963;186:1065–74.[Abstract/Free Full Text]
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Abstract
Introduction
