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Ann Thorac Surg 2000;69:381-387
© 2000 The Society of Thoracic Surgeons

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Original Articles

Bilateral sequential single lung transplantation for pulmonary hypertension and Eisenmenger’s syndrome

^a Heart and Lung Transplant Service, Alfred Hospital, Victoria, Australia

Address reprint requests to Dr. Esmore, Heart and Lung Transplant Service, Commercial Rd, Prahran, Victoria 3181, Australia

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Lung transplantation, with and without intracardiac repair for pulmonary hypertension (PH) and Eisenmenger’s syndrome (EIS), has become an alternative transplant strategy to combined heart and lung transplantation (HLT).

Methods. Thirty-five patients with PH or EIS underwent either bilateral sequential single lung transplantation (BSSLT, group I, n = 13) or HLT (group II, n = 22). Another 74 patients, who underwent BSSLT for other indications, served as controls (group III). Immediate allograft function, early and medium-term outcomes, lung function, and 2-year survival were compared between the groups.

Results. Comparisons between groups I and II showed no significant difference in any variables except percent predicted forced vital capacity. Immediate allograft function was significantly inferior (p < 0.05) and the blood loss was greater (p < 0.01) in group I when compared with those in group III. However, this resulted in no significant difference in early and medium-term outcomes, and 2-year survival between the 2 groups.

Conclusions. BSSLT for PH and EIS can be performed as an alternative procedure to HLT without an increase in early and medium-term morbidity and mortality. Results are comparable with BSSLT performed for other indications.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
In the early experience of thoracic transplantation, combined heart and lung transplantation (HLT) was the only surgical option for patients with pulmonary hypertension (PH) or Eisenmenger’s syndrome (EIS) [1]. However, because of the known improvement in right ventricular dysfunction that follows a postoperative drop in pulmonary vascular resistance [2], and given the scarcity of suitable donor organs, lung transplantation with and without intracardiac repair has evolved as an alternative operation for these patients. The potential problems associated with HLT, including allograft coronary artery disease and differential heart and lung rejection, have also accelerated the acceptance of this new surgical strategy.

At our institution, HLT had been initially performed for the patients with primary PH, EIS, and bilateral infective lung disease. However, based on the scarcity of donor organs, we have changed our surgical strategies for these patients, shifting from HLT to bilateral sequential single lung transplantation (BSSLT) with and without simultaneous repair of congenital cardiac anomalies.

Through this retrospective study, we evaluated the immediate postoperative and medium-term outcomes after BSSLT with and without intracardiac repair for PH or EIS, and compared them with those after HLT for the same operative indications, as well as with those after BSSLT for others indications.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
Between August 1990 and December 1997, 97 BSSLT and 45 HLT were performed at the Alfred Hospital. Included were 13 BSSLT (group I) and 22 HLT (group II) in patients with a diagnosis of PH or EIS, and 74 BSSLT were performed for other indications (group III). Between August 1990 and September 1993, HLT had been performed for the patients of PH. Since reversibility of functionally impaired right ventricle of these patients has been recognized, we have changed our transplant strategy to perform BSSLT instead of HLT unless there is extremely impaired right ventricle function with severe right heart failure. Thirteen patients (9 PPH and 4 EIS) among 22 patients in group II underwent HLT before October 1993 and another 9 patients (1 PPH and 8 EIS) have been done since that time. Patients with other pretransplant diagnoses or incomplete data after transplant (23 HLT and 10 BSSLT) were excluded from this analysis.

Donors’ operation
Donor organ procurement and preservation were standardized. Donor hearts were arrested with 1 L of cold oxygenated Plegisol solution (Travenol; Abbott Laboratory, Abbott Park, Il) with added bicarbonate and aspartate. For donor lungs, prostacyclin (Flolan, Wellcome, Sydney, Australia) was infused at 40 to 80 ng/kg/min for approximately 10 minutes intravenously, and then 4 to 6 L of cold modified Euro-Collins solution was administered at a pressure of 40 cm water through a cannula into the main pulmonary artery. The trachea of donor lungs was stapled after the lungs were inflated with 100% oxygen at a pressure of 5 cm water.

Recipients’ demographics
The recipients’ demographics are presented in Table 1. The ischemic time for groups I and III was the average value of the ischemic time for the first and second transplanted lung. In group II, the ischemic time was the interval between placement of the aortic cross-clamp in the donors’ operation and release of aortic cross-clamp in the recipient operation as both lungs were simultaneously reperfused after the aortic cross-clamp was released.

Postoperative management
For the patients in group III, a midthoracic epidural catheter was inserted before induction of anesthesia and a mixed solution of local anesthetic and narcotic was continuously infused through this catheter for up to 5 days for pain relief, combined with aggressive chest physiotherapy. This allowed smooth weaning from ventilator support. For the patients in groups I and II, pain control by epidural catheter was not performed because of preoperative warfarinization in group I and because of median sternotomy in group II. The modes of ventilator setting were uniformly standardized. Tracheostomy was performed in patients who could not be weaned from the ventilator within 7 days of transplantation.

Immunosuppression and prophylaxis of infection
Patients undergoing transplantation between August 1990 and October 1992 received cytolytic therapy with antithymocyte globulin (Pharmacia and Upjohn Worldwide, Kalamazoo, MI) for 7 to 10 days from the time of transplantation. Cyclosporin and azathioprine were commenced before transplantation and prednisolone added from day 7. Patients undergoing transplantation after October 1992 were not given cytolytic induction, and all commenced triple therapy (cyclosporin, azathioprine, and prednisolone) immediately after operation. Maintenance therapy included cyclosporin (2 to 20 mg/kg/day), azathioprine (1 to 2 mg/kg/day), and prednisolone (0.1 to 0.2 mg/kg/day). Bronchoscopies with biopsy were performed routinely at 2, 4, 8, 12, 26, 39, and 52 weeks and additionally when airway complications or rejection were suspected clinically. Antibiotics with actioning against known or suspected organisms were given intravenously after transplant. The long-term prophylaxis for Pneumocystis carini was achieved with low-dose oral trimethiprim-sulfamethoxazole. Intravenous ganciclovir was used for prophylaxis of cytomegalovirus infection in serologically positive donors or recipients.

Statistical analysis
A computer program package, Statview 4.0 (Abacus Concepts, Berkeley, CA) for Macintosh (Apple Computer, Inc, Cupertino, CA), was used for statistical analysis. Data are presented as mean ± standard deviation. For the duration of ventilation, intensive care unit (ICU) and hospital stays, median values associated with a range of individual data are described. Comparisons between groups I and II or between groups I and III for ratio of arterial oxygen tension to inspired oxygen fraction (PO₂/FiO₂) and alveolar-arterial oxygen gradient (A-aDO₂), percent predicted forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV₁) were made by the repeated 2-way analysis of variance (ANOVA) test. Comparisons for age, ischemic time, blood loss, and follow-up period were made by the unpaired Student’s t-test. Prevalences of reoperation for bleeding, need for tracheostomy, hospital death, overall death, and complications after operation were compared by ² analysis. Actual survival after transplantation was estimated by the Kaplan-Meier method, using the log-rank test.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Pulmonary graft function (PO₂/FiO₂ and A-aDO₂) within the first 24 hours after admission to ICU in the 3 groups is presented in Figures 1 and 2. Postoperative outcomes before discharge from the hospital are shown in Table 2. Medium-term morbidity and mortality after transplant are presented in Table 3. Percent predicted FVC and FEV₁ after transplantation is presented in Figure 3 and survival curves are presented in Figure 4.

View larger version (26K): [in this window] [in a new window]   Fig 1. Changes in PO2/FiO2 after transplantation. Each point represents the mean ± standard deviation. Repeated 2-way ANOVA showed a significant difference between groups I and III (p = 0.02), but no significant difference between groups I and II (p = 0.44). (ANOVA = analysis of variance; PO2/FiO2 = ratio of arterial oxygen tension to inspired oxygen fraction; GI = group I; GII = group II; GIII = group III.)

View larger version (25K): [in this window] [in a new window]   Fig 2. Changes in A-aDO2 after transplantation. Each point represents the mean ± standard deviation. Repeated 2-way ANOVA showed a significant difference between groups I and III (p = 0.01), but no significant difference between groups I and II (p = 0.51). (ANOVA = analysis of variance; A-aDO2 = alveolar-arterial oxygen gradient; GI = group I; GII = group II; GIII = group III.)

View larger version (20K): [in this window] [in a new window]   Fig 3. Percent of predicted FVC (upper) and FEV1 (lower) after transplantation. Repeated 2-way ANOVA showed a significant difference in percent predicted FVC (p = 0.02), but not in percent predicted FEV1 (p = 0.19) between groups I and II. No significant difference was detected in percent predicted FVC (p = 0.25) and FEV1 (p = 0.84) between groups I and III. (FVC = forced vital capacity; FEV1 = forced expiratory volume in 1 second; ANOVA = analysis of variance; GI = group I; GII = group II; GIII = group III.)

View larger version (24K): [in this window] [in a new window]   Fig 4. Two-year survival rate. There was no significant difference in 2-year survival rate at 24 months after transplantation between group I and group II (p = 0.93) or group III (p = 0.89). (GI = group I; GII = group II; GIII = group III).

Group I versus group III
Repeated ANOVA showed that the PO₂/FiO₂ ratio was significantly higher (p = 0.02) and A-aDO₂ was significantly lower (p = 0.01) in group III (GIII) as compared to group I recipients. There was a significant difference in blood loss within 24 hours (p = 0.01, GI 2145 ± 1123 versus GIII 1377 ± 948 mL) between the 2 groups. No significant difference was found in prevalences of reoperation for bleeding (p = 0.16, GI 2 of 13 versus GIII 3 of 74), need for tracheostomy (p = 0.17, GI 5 of 13 versus GIII 15 of 74), and hospital death (p > 0.99, GI 0 of 13 versus GIII 4 of 74). The median durations of ventilation and ICU stay in group I were much longer than those in group III. Pulmonary function testing showed no significant difference in percent predicted FVC (p = 0.25) and FEV₁ (p = 0.84) between the 2 groups. In addition, there was no significant difference in prevalences of airway complications (p = 0.21, GI 2 of 13 versus GIII 27 of 74), BOS (p = 0.16, GI 2 of 13 versus GIII 3 of 74), rejection (p = 0.37, GI 4 of 13 versus GIII 37 of 74), and the prevalence of death from sepsis (p = 0.59, GI 0 of 13 versus GIII 6 of 74) or MOF (p > 0.99, GI 0 of 13 versus GIII 2 of 74) between the 2 groups. The Kaplan-Meier curves showed no significant difference (p = 0.89) in patients’ survival between the 2 groups.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
Single lung transplantation (SLT) was introduced earlier than BSSLT as an alternative to HLT in the management of patients with PH. Pasque and colleagues reported early favorable hemodynamic outcomes and good early survival after SLT in 34 patients [2]. They demonstrated an early and complete normalization of hemodynamics that persisted for at least 4 years after transplantation [2]. However, Bando and coworkers showed that preoperative PH leads to prolonged ICU stay due to unstable hemodynamics, pulmonary edema, and infection with less symptomatic improvement and significantly lower survival [5, 6]. They also pointed out that significant ventilation/perfusion (V/Q) mismatch in SLT recipients with preoperative PH contributed to these unfavorable outcomes [5, 6].

With respect to the avoidance of V/Q mismatch, double lung transplantation (DLT) and BSSLT are the preferred operative procedures for patients with PH rather than SLT, because both pathologic lungs are replaced. An increased incidence of BOS in SLT recipients with PH [7] is suggested to have a negative impact on long-term survival. However, contrary to their previous reports, the same group in Pittsburgh concluded that SLT was the operation of choice for primary and secondary PH, based upon similar long-term outcomes after SLT or DLT in an updated report [8]. However, in their study, 10 of 21 SLT recipients with PH did not survive more than 1 year, including 4 deaths within 30 days after transplantation [8]. With respect to the DLT group for PH, 6 patients of 37 did not survive more than 30 days, associated with twice as long median durations of ICU stay (16 days) and of hospital stay (52 days) [8] as those in our study (6.8 days and 28 days, respectively).

En-bloc DLT was first introduced clinically by the Toronto group and their initial experiences were reported to be excellent [9]. However, further experience demonstrated several postoperative problems following en-bloc DLT. Cooper showed several limitations of en-bloc DLT: (1) very complex procedures, (2) significant postoperative cardiac dysfunction associated with the need for cardiac arrest, and (3) variable degrees of cardiac denervation due to the mediastinal dissection [10]. BSSLT is technically easier than en-bloc DLT. It is not necessary to arrest the heart in BSSLT unless combined with intracardiac repair for the patients with EIS. Cardiac denervation is not a concern in BSSLT. In addition, the transverse and bilateral thoracosternotomy can provide superb exposure of both thoracic cavities from apex to diaphragm.

Chapelier and associates [11] described several disadvantages of BSSLT when compared with en-bloc DLT: 1) risk of bronchial artery fistula or intrapleural dehiscence, 2) shift of total pulmonary flow to the first transplanted lung during implantation of the second lung, and 3) prolonged graft ischemic time in the second lung. In addition, they described one of the advantages of en-bloc DLT over BSSLT: it allows faster and simultaneous reperfusion to both lungs.

However, in our experience, we have not observed symptomatic bronchial artery fistula, either in group I or III. Dehiscence after tracheal or bilateral proximal bronchial anastomosis in the mediastinum and its consequent mediastinitis may be a more life-threatening and devastating complication than intrapleural bronchial dehiscence. Consequently, under CPB support, the first transplanted lung did not receive total pulmonary flow during implantation of the second lung. The longer ischemic time of the second transplanted lung in group I might have contributed, to some extent, to inferior gas exchange capacity expressed as PO₂/FiO₂ and A-aDO₂ at the initial data point in group I, but 6 hours later, the gas exchange capacity in group I had become almost identical to that in group II. Pasque and colleagues [12] found that a decrease in perfusion in the second lung, on immediate postoperative scan, improved remarkably on the following day. In fact, the temporary drop in pulmonary function immediately after operation in group I did not have any negative impact on morbidity and mortality during admission and after discharge from the hospital.

We have expanded the indication of BSSLT with correction of congenital cardiac anomalies to the patients with EIS. Since the report of SLT with repair of congenital anomalies from Fremes and colleagues [13], this new surgical strategy has been followed by the others with successful symptomatic improvement in the early postoperative period [14]. However, Lupinetti and associates [15] reported less favorable long-term results after SLT with correction of congenital cardiac anomalies despite good survival through the first postoperative year. The overwhelming shift of blood flow to the transplanted lung may contribute to the late deterioration of graft function and to a lower survival rate. Based upon these theoretical advantages and observed clinical outcomes, replacement of both pathologic lungs may possibly be a more appropriate procedure for the patients with PH due to congenital anomalies. We have experienced two cases of BSSLT combined with closure of ASD and found no additional intraoperative and postoperative problems associated with ASD closure.

Although the amount of blood loss within 24 hours after operation and need for tracheostomy in group I was slightly, but not significantly, greater than those in group II, they did not cause a great difference in early morbidity and mortality between groups I and II. Our results demonstrated that BSSLT with or without correction of congenital anomalies could be performed without increased morbidity and mortality for the patients with PH or EIS, who had previously been regarded as candidates for HLT only. This allowed donor hearts to be used for other recipients and avoided the risk of differential rejection. However, we still believe that HLT, rather than BSSLT with intracardiac repair, would be indicated for the patients with EIS caused by more complex congenital anomalies, which are irrepairable or expected to require a much longer aortic cross-clamping time for their correction.

When compared with group III, we found significantly greater blood loss within 24 hours in ICU in group I. There are several possible explanations. Twelve patients of 13 in group I had taken warfarin up until the day of transplantation. Additionally, it is mandatory to use CPB for these patients, so since the average CPB time in group I was prolonged at 261 minutes, it is not surprising that a coagulopathy had occurred and continued in the early stages after operation. The combination of pretransplant warfarinization and prolonged CPB might have contributed to a trend toward increased postoperative bleeding.

Significant blood loss consequently required supplemental transfusion of packed blood cells, fresh frozen plasma, and platelet products. It is well known that transfusing large amount of blood products can induce further deterioration of pulmonary gas exchange. Aeba and colleagues [16] demonstrated that the use of CPB in lung transplantation significantly contributed to lower mean arterial to alveolar oxygenation ratio, higher graft injury scores of chest radiographs, and a longer intubation period. This may be one possible explanation of why early posttransplant allograft function was significantly inferior and the need for tracheostomy was relatively higher in group I in comparison to that in group III.

Additionally, the lack of respiratory muscle loading and subsequent training effect in patients with PH and EIS, compared with non-PH patients, could be another possible explanation for prolonged ventilation and greater need for tracheostomy in group I. Levine and colleagues demonstrated cellular adaptations in the diaphragm of the patients with chronic obstructive pulmonary disease, consisting of an increased proportion of less-fatigable slow twitch muscle fibers and slow isoforms of myofibrillar proteins [17]. These cellular changes might have contributed to earlier weaning from ventilator in group III where all patients will have some chronic respiratory muscle training, due to their underlying diseases. The avoidance of epidural catheter insertion, because of fear of potential epidural bleeding related to warfarin therapy, might have caused further delay in extubating the patients in group I.

In this study, there was no statistically significant difference in the incidences of reoperation for bleeding, results of posttransplant pulmonary function tests, prevalences of rejection, airway complication, BOS, sepsis, and MOF between groups I and III. According to the official report by International Society for Heart and Lung Transplantation [18] and the other individual centers [6, 11], 1-year and 2-year survival rates after DLT or BSSLT for patients with PH were lower than those in patients with the other indications. The total number of patients in group I was small, and although the 2-year survival of this group was encouraging, it is not statistically different from that of group III.

In conclusion, BSSLT with and without repair of relatively simple congenital cardiovascular anomalies is a viable alternative transplant procedure to HLT for the patients with PH or EIS. Despite greater postoperative blood loss, longer periods of ventilation and ICU stay, and a greater need for tracheostomy in group I, we have shown that this strategy could be performed without significant increase in morbidity and mortality both in the early and medium posttransplant period even when compared with those of BSSLT for other indications.

	References

Top Abstract Introduction Patients and methods Results Comment References

 

1. Griffith B.P., Hardesty R.L., Trento A., et al. Heart-lung transplantation. Ann Thorac Surg 1987;43:6-16.[Abstract]
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3. Reitz B.A. Heart and lung transplantation. In: Baumgartner W.A., Reitz B.A., Achuff S.C., eds. Heart and heart-lung transplantation. Philadelphia: WB Saunders, 1990:313-346.
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7. Kshettry V.R., Kroshus T.J., Savik K., Hertz M.I., Bolman R.M. Primary pulmonary hypertension as a risk factor for the development of obliterative bronchiolitis in lung allograft recipients. Chest 1996;110:704-709.[Abstract/Free Full Text]
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13. Fremes S.E., Patterson G.A., Williams W.G., et al. Single-lung transplantation and closure of patent ductus arteriosus for Eisenmenger’s syndrome. J Thorac Cardiovasc Surg 1990;100:1-5.[Abstract]
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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Julian A. Smith Marc Rabinov Donald S. Esmore Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ueno, T. Articles by Esmore, D. S. Search for Related Content PubMed PubMed Citation Articles by Ueno, T. Articles by Esmore, D. S.