Perioperative changes in lung re-transplantation: a single-centre observational study

Introduction

Background

Assessment for long-term survival of lung transplantation (LTx) has been commenced in the early 1980s in Toronto (1). Since then, LTxs have become the final treatment for end-stage pulmonary disease. With improvements in immunosuppressive drugs, surgical techniques, and postoperative therapy regimens, the overall median survival of LTx patients has improved (2,3). Still, it remains 6.7 years shorter than that of other solid organ transplantations (4,5).

Lung re-transplantation (Re-LTx) is the only available therapy option for severe graft dysfunction (6), but the number of Re-LTx cases is low. Since 2000, of the annual LTx cases worldwide, only 3–5% are Re-LTxs (7,8), which is considerably lower than that for secondary transplantation of the kidney, liver, or heart (9). However, the number of primary LTxs performed is increasing; consequently, the number of patients undergoing Re-LTx has nearly tripled over the past two decades, to approximately 200 cases per year (10). However, the development of Re-LTx in China has lagged. From 2015 to 2018, Re-LTxs accounted for 2.1% of all LTxs in China annually, which is lower than that reported at the international level during the same period (11).

Rationale and knowledge gap

Re-LTxs are complex. Although recent reports indicate that the 1- and 5-year survival rates of Re-LTx are similar to those of primary LTx (12-16), the 5-year survival rate is still low (37%) (17), with a median survival time of 2.5 years (18). A previous study compared the characteristics and survival of patients who underwent Re-LTx and primary LTx (19); however, it did not evaluate intraoperative changes between the two, which directly affects postoperative rehabilitation. Therefore, summarising the key perioperative changes associated with Re-LTx is also important.

Objective

This single-centre, retrospective, propensity score-matched study compared the intraoperative characteristics and treatment schemes of LTx and Re-LTx to guide perioperative management strategies. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1460/rc).

Methods

Study design

This study retrospectively analysed the clinical characteristics of patients who underwent LTx in the First Affiliated Hospital of Guangzhou Medical University from January 1, 2016, to December 31, 2023, including those who underwent Re-LTx. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the institutional ethics board of the First Affiliated Hospital of Guangzhou Medical University (No. ES-2024-104-02) and individual consent for this retrospective analysis was waived. All donor organs are legally obtained through the distribution of the National Organ Allocation Center, and the Chinese Government rejects the illegal use of stolen organs from political and religious prisoners.

Patients >18 years old who underwent LTx at our hospital were included. Patients undergoing combined multiple organ transplantation, those undergoing LTx under cardiopulmonary bypass, donors of ex vivo lung perfusion (EVLP), and paediatric patients were excluded. Patients with incomplete perioperative data were also excluded.

Data collection

Clinical data were collected through the hospital information system, including body mass index (BMI), gender, age, primary disease, comorbidities, the Acute Physiology and Chronic Health Evaluation (APACHE) score, left ventricular ejection fraction (LVEF), the incidence of preoperative mechanical ventilation, and the incidence of extracorporeal membrane oxygenation (ECMO) support. The intraoperative data included the types of LTx, incidence of intraoperative ECMO support, norepinephrine dosage, time of surgery and anaesthesia, blood loss, the infusion volume of red blood cells (RBCs) and plasma, and the intraoperative haemodynamic variables. The postoperative data included the incidence of postoperative ECMO support, length of stay in the intensive care unit (ICU), postoperative hospital stay, total hospital stay, and postoperative complications within seven days. Perioperative laboratory examinations included blood cell counts, coagulation function, and blood gas analyses.

Study outcomes

The primary outcome was to summarise the key points of the intraoperative characteristics of Re-LTx. The secondary outcome was to summarise the short-term postoperative rehabilitation characteristics.

Statistical analyses

Patients who underwent Re-LTx were propensity score-matched with those who underwent primary-LTx at a 1:2 ratio based on age, BMI, gender, primary disease, and transplantation type.

The variable was excluded once the missing data exceeded 10%. Continuous normally distributed numerical variables were expressed as means and standard deviations, and skewed distribution data were expressed as medians (interquartile ranges). Categorical variables were expressed as percentages. Quantitative indicators were compared between groups using two independent sample t-tests or nonparametric rank sum tests based on the data distribution, and a one-way analysis of variance were performed within-group comparisons. The chi-squared test or exact probability method (if the chi-squared test was not applicable) was used for classification indicators. Correlations between variables were analysed using correlation and partial correlation analyses. SPSS version 25.0 (IBM Corp., Armonk, NY, USA) was used for all statistical analyses. Unless otherwise specified, two-sided tests were used for all statistical analyses. P values of <0.05 (two-sided) were considered statistically significant.

Results

The study included 26 patients who underwent primary-LTx who were matched (1:2) with 13 patients who underwent Re-LTx; thus, 39 patients were included in total (Figure 1). The average interval between the two LTxs was 3.55 years.

Figure 1 The flow chart of study. LTx, lung transplantation; CPB, cardiopulmonary bypass; EVLP, ex vivo lung perfusion; Re-LTx, lung re-transplantation; BMI, body mass index.

Age (57.73 vs. 57.38 years), BMI (21.07 vs. 20.63 kg/m²), gender (male 92.3% vs. 92.3%), primary disease, LVEF value (69.04% vs. 68.62%), the incidence of preoperative mechanical ventilation and ECMO support (23.1% vs. 15.4% and 11.5% vs. 15.4%), did not differ between the primary-LTx and Re-LTx groups (P>0.05). However, the diabetes mellitus was higher in the Re-LTx group (46.2% vs. 11.5%, P=0.03), and the preoperative APACHE values were higher in the Re-LTx group than that of the primary-LTx group (22.0 vs. 7.5, P=0.001; Table 1).

The transplantation type (double-LTx 69.2% vs. 69.2%), incidence of intraoperative ECMO support (57.7% vs. 53.8%), dosage of vasoactive drugs, time of surgery and anaesthesia (482.88 vs. 444.23 and 623.35 vs. 566.31 min), blood loss (1,550 vs. 500 mL), and infusion volume of RBC and plasma (1,200 vs. 1,600 and 975 vs. 800 mL), did not differ between the Re-LTx and primary-LTx groups (P>0.05; Table 2).

The incidence of postoperative ECMO support (30.8% vs. 46.2%), the ICU stay (11.5 vs. 12 days), the duration of postoperative hospital stay (28 vs. 30 days), total hospital stay (30.5 vs. 44 days), and the duration of postoperative mechanical ventilation (8 vs. 4 days), did not differ between the primary-LTx and Re-LTx groups (P>0.05). The incidence of one-year survival was also comparable between the two groups (65.4% vs. 69.2%, P=0.81), while the complications without postoperative seven days were lower in the Re-LTx group (30.8% vs. 57.7%, P=0.049) (Table 3).

The white blood cell (WBC) count and neutrophil ratio did not differ between the two groups (P>0.05), while the intraoperative haemoglobin level was significantly lower in the Re-LTx group than the level in the LTx group (P=0.002). On postoperative day three, the WBC count and neutrophil ratio were significantly higher in both groups when compared to the preoperative values (primary-LTx group: P<0.001 and P<0.001; Re-LTx group: P=0.001 and P=0.001), but the intraoperative and postoperative day three haemoglobin levels were significantly lower than the preoperative levels in both groups (primary-LTx group: P=0.005 and P<0.001; Re-LTx: P=0.008 and P=0.03, respectively; Figure 2).

Figure 2 The perioperative changes in blood examination. ^##P<0.01, primary-LTx group vs. Re-LTx group. *P<0.05, **P<0.01, compared with preoperative values primary-LTx group. ^&P<0.05, ^&&P<0.01, compared with preoperative values in Re-LTx group. LTx, lung transplantation; Re-LTx, lung re-transplantation; WBC, white blood cell.

The pH, arterial oxygen pressure (PaO₂), and partial pressure of carbon dioxide (PaCO₂) were comparable between the groups (P>0.05). However, the PaCO₂ values on day three postoperatively were lower than preoperative ones in both groups (primary-LTx: P<0.001; Re-LTx: P=0.02). The post-anaesthesia PaO₂ value was higher than the preoperative ones in the Re-LTx group (P<0.001) but significantly lower than the preoperative value in the primary-LTx group (P=0.001) (Figure 3).

Figure 3 The perioperative changes in blood gas analysis. **P<0.01, compared with preoperative values in primary-LTx group. ^&P<0.05, ^&&P<0.01, compared with preoperative values in Re-LTx group. LTx, lung transplantation; Re-LTx, lung re-transplantation; PaCO₂, partial pressure of carbon dioxide; PaO₂, arterial oxygen pressure.

The values of blood urea nitrogen (BUN) and serum creatinine (SCr) were higher in the Re-LTx group than the values of BUN and SCr in the primary-LTx group before and during surgery (both P<0.01). The values of BUN and SCr on postoperative day three were higher than the preoperative ones in both groups (all P<0.05) (Figure 4).

Figure 4 The perioperative changes in renal function. ^#P<0.05, ^##P<0.01 primary-LTx group vs. Re-LTx group. **P<0.01, compared with preoperative values in primary-LTx group. ^&P<0.05, ^&&P<0.01, compared with preoperative values in Re-LTx group. LTx, lung transplantation; Re-LTx, lung re-transplantation.

The activated partial thromboplastin time (APTT), prothrombin time (PT), and D2-polymer levels did not differ between the two groups (P>0.05), but the fibrinogen level was significantly higher in the primary-LTx group than that of the Re-LTx group after anaesthesia and during surgery (P=0.04 and P=0.03, respectively). The intraoperative and postoperative day three PT, intraoperative APTT, and postoperative day three D2-polymer values were higher than the preoperative values in both groups (all P<0.05). On the contrary, the intraoperative fibrinogen levels were lower than the preoperative ones in both groups (both P=0.001) (Figure 5).

Figure 5 The perioperative changes in coagulation function. ^#P<0.05, primary-LTx group vs. Re-LTx group. *P<0.05, **P<0.01, compared with preoperative values in primary-LTx group. ^&P<0.05, ^&&P<0.01, compared with preoperative values in Re-LTx group. LTx, lung transplantation; Re-LTx, lung re-transplantation; APTT, activated partial thromboplastin time.

The haemodynamic parameters were comparable between the two groups during the perioperative period (P>0.05). When compared with the preoperative values, the mean arterial pressure (MAP), pulmonary artery systolic pressure (PASP), and transcutaneous oxygen saturation (SpO₂) values did not fluctuate significantly after anaesthesia, during the operation, or at the end of the operation (all P>0.05). However, the heart rate at the end of the operation was higher than the preoperative value in the primary-LTx group (P=0.049) (Figure 6).

Figure 6 The perioperative changes in hemodynamics. *P<0.05, compared with preoperative values in primary-LTx group. ^&P<0.05, compared with preoperative values in Re-LTx group. LTx, lung transplantation; Re-LTx, lung re-transplantation; HR, heart rate; MAP, mean arterial pressure; PASP, pulmonary artery systolic pressure; SpO₂, transcutaneous oxygen saturation.

Discussion

Key findings

The perioperative management of LTx is crucial for patient prognosis, particularly in Re-LTx recipients. In the Re-LTx group, the intraoperative APACHE score was significantly higher, the intraoperative haemoglobin level was lower, and the perioperative BUN and SCr levels were higher. However, the intraoperative conditions and postoperative rehabilitation were comparable between the groups, while the complications within postoperative seven days were higher in the Re-LTx group.

Strengths and limitations

There are several limitations in this study. First, the retrospective study design does not completely avoid selection and information biases. However, single center observation is beneficial for homogenized perioperative management processes, with high consistency in inclusive data, and in advantage to eliminate bias from multiple centers. Second, sample heterogeneity was observed. However, despite the small sample capacity and rarity of Re-LTx, a propensity score matching analysis was applied to minimise the bias in basic characteristics between the groups. Third, follow-ups were mostly performed during postoperative hospitalisation, and the evaluation of long-term effects was insufficient. But one-year survival incidence of Re-LTx was clarified.

Explanations of findings and comparison with similar research

Recipient age, BMI, and transplantation type are high-risk factors for 1- and 5-year survival of Re-LTx (20). Therefore, we conducted a propensity score matching analysis based on these factors. In this study, most patients undergoing Re-LTx were patients with nonspecific interstitial pneumonia (42.3%), followed by idiopathic pulmonary fibrosis (26.9%) and chronic obstructive pulmonary disease (15.4%), which is analogous to the proportions reported by Hall et al. (21). Compared to primary LTx, the likelihood of death from Re-LTx increases by 30% (20). Furthermore, ECMO assistance during Re-LTx is associated with a high mortality risk (22). In this study, the proportions of preoperative mechanical ventilation and ECMO assistance were similar between the primary-LTx and Re-LTx groups, consistent with the findings of Wallinder et al. (23). However, a large retrospective analysis by Chan et al. (24) that included 5,301 primary-LTx and 277 Re-LTx cases found that more patients in the Re-LTx group than in the primary-LTx group received preoperative mechanical ventilation and ECMO bridging. Thomas et al. reported similar results (25), but our results were inconsistent with those findings. We did, however, find higher preoperative APACHE II scores in the Re-LTx group than in the LTx group. The higher the APACHE score, the more complications in Re-LTx, mainly concentrated in hemorrhage and acute kidney injury (AKI). And the mortality within postoperative 7 days was also higher. Therefore, this suggested that the organ function and physiological indicators were worse in the Re-LTx group than those in the primary-LTx group. Improving preoperative organ function is crucial for prognosis in Re-LTx, and intraoperative and postoperative monitoring and treatment should be improved.

The proportion of patients on intraoperative ECMO support and the dosages of vasoactive drug were similar in the Re-LTx and primary-LTx groups, and the intraoperative haemodynamic parameters were stable in both groups. These indicated that during the perioperative period, the haemodynamic management of Re-LTx was the same as that of primary LTx. Notably, the volume of blood loss was lower in the Re-LTx group than that in the primary-LTx group (800 vs. 1,550 mL) even though a higher amount of blood transfusion was required. A retrospective analysis of the data showed that patients who underwent Re-LTx had lower preoperative haemoglobin levels and moderate to severe anaemia. A partial correlation analysis was performed to control the preoperative haemoglobin level and analyse the volume of blood transfusion and bleeding, resulting in a correlation coefficient between blood transfusion and bleeding volume of 0.928. Thus, after excluding the influence of haemoglobin, the positive correlation between blood transfusion and bleeding volume strengthened, meaning the preoperative haemoglobin level affected the intraoperative amount of blood transfusions. In addition, the surgical time was also similar between the two groups, but the surgical procedure is more difficult for Re-LTx than for primary LTx. The intraoperative fibrinogen levels were low in the Re-LTx group, suggesting decreased coagulation function. These factors could have contributed to lower intraoperative haemoglobin levels in the Re-LTx group, resulting in a higher blood transfusion volume requirement. Therefore, preoperative oral iron promotes the production of hemoglobin, while intraoperative enhancement of coagulation function reduces bleeding.

The survival rates of LTx at 1-, 3- and 5-year are 82.2%, 68.1%, and 55.6%, respectively (26), and the survival rates of Re-LTx at 1-, 2-, and 3-year are 47%, 40%, and 33%, respectively (27). The Re-LTx survival rates are lower than that of other solid organ transplantations (19), and the Re-LTx mortality is significantly higher than that of primary LTx. Therefore, postoperative rehabilitation is closely related to LTx survival (2,28). Halloran et al. found that patients who underwent Re-LTx had an increased postoperative duration of ventilator use compared to those who underwent primary LTx, which increased the length of the ICU stay (29). However, this contradicts the findings of other case reports and our results (23,30). We did collect data on the postoperative duration of ventilator assistance; however, in our study, the postoperative duration of mechanical ventilation had no statistical difference between groups. The postoperative ECMO support, the postoperative hospital stay, total hospital stay, and postoperative ICU stay, were also comparable between the two groups, analogous to the results of Biswas Roy et al. (30). Furthermore, the incidence of one-year survival was nearly equal in the Re-LTx and primary-LTx groups. Therefore, the patient’s recovery after Re-LTx was similar to primary-LTx, which was also confirmed by the report of Schäfers et al. (31). However, the incidence of complications within postoperative day seven was higher in Re-LTx patients, especially in hemorrhage and AKI, which may be due to the complex procedures of Re-LTx and the impact of preoperative anti-rejection drugs. In our study, patients undergoing Re-LTx had an average interval of 3.55 years between the first and second LTx, which was less than the 4.17 years reported by Lindstedt et al. (32). Whether Re-LTx is as beneficial as primary LTx, which is raised by Biswas and Osho (30,33), still needs more clinical data to support it.

In this study, the preoperative levels of SCr and BUN in the Re-LTx group were higher than those in the LTx group. Patients use glucocorticoids, nucleotide synthesis inhibitors (mycophenolate mofetil), and calcineurin inhibitors (tacrolimus) for anti-rejection treatment after LTx (30). Therefore, renal function injury caused by long-term anti-rejection therapy is predictable. Wallinder et al. (23) reported that diabetes and an impaired glomerular filtration rate are common complications of long-term immunosuppressive therapy. Additionally, since calcineurin inhibitors are commonly used for standard maintenance immunosuppression, renal function is almost always impaired during re-transplantation (31,34). We found that high levels of BUN and SCr persisted until the third postoperative day, which were mostly attributable to the preoperative renal function injured by pre-transplantation and the exposure to pre-existing calcineurin-inhibitors (31); thus, patients undergoing Re-LTx may need earlier perioperative renal protection. Although some have reported that the SCr level does not predict survival after re-transplantation (19,35), the annual report by the International Society for Heart and Lung Transplantation identified several factors associated with an increase in 1-year mortality after LTx, including an elevated SCr level (1). Nonetheless, the effect of creatinine on survival after LTx remains an area of future research.

The perioperative PaCO₂ and PaO₂ values also did not differ between the primary-LTx and Re-LTx groups in this study, indicating that pulmonary gas exchange functioned comparably between the two groups. This result aligns with that regarding the similar incidence of intraoperative ECMO support. The perioperative coagulation functions were also comparable between the groups, resulting in similar total transfusion volumes in both groups.

Implications and actions needed

The intraoperative conditions, including blood loss and transfusion volumes, intraoperative haemodynamic parameters, pulmonary gas exchange, and postoperative rehabilitation, were comparable between LTx and Re-LTx groups, indicating that the management strategies for intraoperative haemodynamics and ventilation were consistent in primary and re-transplantation patients. However, patients who undergo Re-LTx are prone to anaemia and renal dysfunction. Therefore, early renal protection and renal replacement therapies should be implemented. Meanwhile, more Re-LTx patients were combined with diabetes. Whether diabetes can affect the prognosis of LTx needs more clinical data or prospective research to confirm. In addition, attention should be paid to maintaining perioperative coagulation to avoid aggravating bleeding. Proper blood transfusions should be administered to correct anaemia and ensure oxygenation in patients receiving Re-LTx. Finally, with advances in immunosuppressive therapy, preservation of donor organs, and technological improvement in extracorporeal perfusion to improve donor lung function, cases of Re-LTx will gradually go higher. Establishing global data-sharing in advance will benefit the scarce Re-LTx patients in obtaining better perioperative management, improving prognosis, and prolonging the lifespan.

Conclusions

We retrospectively analysed the perioperative characteristics and changes between patients undergoing primary and Re-LTx, finding similar intraoperative conditions and postoperative rehabilitation characteristics, even for intraoperative pulmonary gas exchange and the haemodynamic parameters. These results suggest that the same perioperative management could be provided to primary and re-transplantation patients. However, renal protection measures should be applied earlier, and attention should be paid to correcting anaemia in patients undergoing Re-LTx.

Acknowledgments

The authors are pleased to acknowledge all resident doctors who participated in the collection and assembly of data.

Funding: This study was supported by Guangzhou Municipal Science and Technology Bureau, The Project of Basic and Applied Basic Research Jointly Funded by Municipality and University (Hospital) (Fund No. 202201020584).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1460/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1460/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1460/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1460/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the institutional ethics board of the First Affiliated Hospital of Guangzhou Medical University (No. ES-2024-104-02) and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Patterson GA, Cooper JD, Goldman B, et al. Technique of successful clinical double-lung transplantation. Ann Thorac Surg 1988;45:626-33. [Crossref] [PubMed]
2. Hayes D Jr. A review of bronchiolitis obliterans syndrome and therapeutic strategies. J Cardiothorac Surg 2011;6:92. [Crossref] [PubMed]
3. Keshavjee S. Retransplantation of the lung comes of age. J Thorac Cardiovasc Surg 2006;132:226-8. [Crossref] [PubMed]
4. Yusen RD, Edwards LB, Dipchand AI, et al. The Registry of the International Society for Heart and Lung Transplantation: Thirty-third Adult Lung and Heart-Lung Transplant Report-2016; Focus Theme: Primary Diagnostic Indications for Transplant. J Heart Lung Transplant 2016;35:1170-84. [Crossref] [PubMed]
5. Chambers DC, Cherikh WS, Harhay MO, et al. The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: Thirty-sixth adult lung and heart-lung transplantation Report-2019; Focus theme: Donor and recipient size match. J Heart Lung Transplant 2019;38:1042-55. [Crossref] [PubMed]
6. Sakornpant P, Kasemsarn C, Yottasurodom C. Retransplantation after single lung transplantation. Transplant Proc 2008;40:2617-9. [Crossref] [PubMed]
7. Jin X, Vanluyten C, Orlitová M, et al. Off-pump lung re-transplantation avoiding clamshell thoracotomy is feasible and safe: a single-center experience. J Thorac Dis 2023;15:5811-22. [Crossref] [PubMed]
8. Godinas L, Van Raemdonck D, Ceulemans LJ, et al. Lung retransplantation: walking a thin line between hope and false expectations. J Thorac Dis 2019;11:E200-3. [Crossref] [PubMed]
9. Khush KK, Cherikh WS, Chambers DC, et al. The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: Thirty-sixth adult heart transplantation report - 2019; focus theme: Donor and recipient size match. J Heart Lung Transplant 2019;38:1056-66. [Crossref] [PubMed]
10. Rucker AJ, Nellis JR, Klapper JA, et al. Lung retransplantation in the modern era. J Thorac Dis 2021;13:6587-93. [Crossref] [PubMed]
11. Magee JC, Barr ML, Basadonna GP, et al. Repeat organ transplantation in the United States, 1996-2005. Am J Transplant 2007;7:1424-33. [Crossref] [PubMed]
12. Aigner C, Jaksch P, Taghavi S, et al. Pulmonary retransplantation: is it worth the effort? A long-term analysis of 46 cases. J Heart Lung Transplant 2008;27:60-5. [Crossref] [PubMed]
13. Brugière O, Thabut G, Castier Y, et al. Lung retransplantation for bronchiolitis obliterans syndrome: long-term follow-up in a series of 15 recipients. Chest 2003;123:1832-7. [Crossref] [PubMed]
14. Martinu T, Howell DN, Davis RD, et al. Pathologic correlates of bronchiolitis obliterans syndrome in pulmonary retransplant recipients. Chest 2006;129:1016-23. [Crossref] [PubMed]
15. Osaki S, Maloney JD, Meyer KC, et al. Redo lung transplantation for acute and chronic lung allograft failure: long-term follow-up in a single center. Eur J Cardiothorac Surg 2008;34:1191-7. [Crossref] [PubMed]
16. Strueber M, Fischer S, Gottlieb J, et al. Long-term outcome after pulmonary retransplantation. J Thorac Cardiovasc Surg 2006;132:407-12. [Crossref] [PubMed]
17. Dipchand AI, Edwards LB, Kucheryavaya AY, et al. The registry of the International Society for Heart and Lung Transplantation: seventeenth official pediatric heart transplantation report--2014; focus theme: retransplantation. J Heart Lung Transplant 2014;33:985-95. [Crossref] [PubMed]
18. Vaquero Barrios JM, Santos Luna F, Salvatierra Velázquez Á. Lung Re-Transplantation. The Opposite View Point. Arch Bronconeumol (Engl Ed) 2018;54:311-2. [Crossref] [PubMed]
19. Kawut SM, Lederer DJ, Keshavjee S, et al. Outcomes after lung retransplantation in the modern era. Am J Respir Crit Care Med 2008;177:114-20. [Crossref] [PubMed]
20. Hayanga JA, Yang J, Aboagye J, et al. Risk factors associated with lung retransplantation: evaluation of a nationwide registry over a quarter century. Ann Thorac Surg 2014;98:1742-6; discussion 1746-7. [Crossref] [PubMed]
21. Hall DJ, Belli EV, Gregg JA, et al. Two Decades of Lung Retransplantation: A Single-Center Experience. Ann Thorac Surg 2017;103:1076-83. [Crossref] [PubMed]
22. Hayes D Jr, Higgins RS, Kilic A, et al. Extracorporeal membrane oxygenation and retransplantation in lung transplantation: an analysis of the UNOS registry. Lung 2014;192:571-6. [Crossref] [PubMed]
23. Wallinder A, Danielsson C, Magnusson J, et al. Outcomes and Long-term Survival After Pulmonary Retransplantation: A Single-Center Experience. Ann Thorac Surg 2019;108:1037-44. [Crossref] [PubMed]
24. Chan EG, Hyzny EJ, Ryan JP, et al. Outcomes following lung re-transplantation in patients with cystic fibrosis. J Cyst Fibros 2022;21:482-8. [Crossref] [PubMed]
25. Thomas M, Belli EV, Rawal B, et al. Survival After Lung Retransplantation in the United States in the Current Era (2004 to 2013): Better or Worse? Ann Thorac Surg 2015;100:452-7. [Crossref] [PubMed]
26. Valapour M, Skeans MA, Heubner BM, et al. OPTN/SRTR 2012 Annual Data Report: lung. Am J Transplant 2014;14:139-65. [Crossref] [PubMed]
27. Novick RJ, Stitt LW, Al-Kattan K, et al. Pulmonary retransplantation: predictors of graft function and survival in 230 patients. Pulmonary Retransplant Registry. Ann Thorac Surg 1998;65:227-34. [Crossref] [PubMed]
28. Schumer EM, Rice JD, Kistler AM, et al. Single Versus Double Lung Retransplantation Does Not Affect Survival Based on Previous Transplant Type. Ann Thorac Surg 2017;103:236-40. [Crossref] [PubMed]
29. Halloran K, Aversa M, Tinckam K, et al. Comprehensive outcomes after lung retransplantation: A single-center review. Clin Transplant 2018;32:e13281. [Crossref] [PubMed]
30. Biswas Roy S, Panchanathan R, Walia R, et al. Lung Retransplantation for Chronic Rejection: A Single-Center Experience. Ann Thorac Surg 2018;105:221-7. [Crossref] [PubMed]
31. Schäfers HJ, Hausen B, Wahlers T, et al. Retransplantation of the lung. A single center experience. Eur J Cardiothorac Surg 1995;9:291-5; discussion 296. [Crossref] [PubMed]
32. Lindstedt S, Dellgren G, Iversen M, et al. Pulmonary retransplantation in the Nordic countries. Ann Thorac Surg 2015;99:1781-7. [Crossref] [PubMed]
33. Osho AA, Castleberry AW, Snyder LD, et al. Differential outcomes with early and late repeat transplantation in the era of the lung allocation score. Ann Thorac Surg 2014;98:1914-20; discussion 1920-1. [Crossref] [PubMed]
34. Michel E, Galen Hartwig M, Sommer W. Lung Retransplantation. Thorac Surg Clin 2022;32:259-68. [Crossref] [PubMed]
35. Shuhaiber JH, Kim JB, Hur K, et al. Survival of primary and repeat lung transplantation in the United States. Ann Thorac Surg 2009;87:261-6. [Crossref] [PubMed]