Off-pump lung re-transplantation avoiding clamshell thoracotomy is feasible and safe: a single-center experience

Introduction

Chronic lung allograft dysfunction (CLAD), including bronchiolitis obliterans syndrome (BOS) and restrictive allograft syndrome (RAS), is the main cause hindering the long-term survival of lung transplant (LTx) patients (1). Lung re-transplantation (re-LTx) is the only viable option in selected patients with severe CLAD comprising about 5% of the annual LTx activity worldwide. Considering the patient’s status and previous thoracic surgical intervention(s), re-LTx is usually more complex than the initial LTx procedure. Therefore, 1-year patient survival of re-LTx patients is 78%, which seems less than the internationally reported 85% of primary LTx (2-5).

Due to the limited number of patients and reported experience, the criteria for patient selection and surgical approach in re-LTx are debatable and center-dependent. Due to expected severe adhesions and difficulty in exposure following previous thoracotomy, the clamshell approach and the use of extracorporeal life support (ECLS) could be preferred for re-LTx procedures (6-8). However, this more invasive approach comes with related complications (bleeding, thrombosis, sternal malunion and wound problems, etc.). Limited experience with off-pump clamshell-avoiding re-LTx has been reported.

At the University Hospitals Leuven, the general routine in primary sequential single-lung transplantation (Tx) is the off-pump technique through a bilateral anterior thoracotomy. We aim to retrospectively analyze our surgical experience and short- and long-term outcomes after re-LTx comparing the less invasive to the more invasive approach, illustrating the feasibility and safety of off-pump clamshell-avoiding re-LTx.

Methods

We performed a single-center retrospective cohort study including all patients undergoing re-LTx at the University Hospitals Leuven (UZ Leuven), Belgium between January 2007 and December 2021. The exclusion criteria were patients with incomplete data, multi-organ transplant or single re-LTx. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee UZ/KU Leuven (No. S51577). There is no experiment in this paper as it is a retrospective study of clinical strategies, therefore informed consent is not required.

Demographics and outcomes

Donor data [type, age, gender, cause of death, and partial pressure of oxygen to fraction of inspiratory oxygen (PaO₂/FiO₂) ratio] were collected from the donor report. Recipient characteristics [including gender, age at (re-)LTx, years between the initial LTx and re-LTx, body mass index (BMI), and days on the waiting list), indication for re-LTx, the ratio of preoperative forced expiratory volume in 1 second/forced vital capacity (FEV1%), the ratio of forced vital capacity/prediction (FVC%), 6-minute walking distance (6MWD), cytomegalovirus (CMV) and Epstein-Barr virus (EBV) status, human leukocyte antigen (HLA) mismatch, panel reactive antibody (PRA), complement-dependent cytotoxic (CDC)-crossmatch, post-re-LTx donor-specific antibodies (DSA)], short-term outcome [operative time, ECLS application, grade 3 primary graft dysfunction (PGD-3) within and at 72-h post-transplant, mechanical ventilation in days, intensive care unit (ICU) and hospital stay, 90-day reoperation incidence], and long-term outcome (1- and 5-year patient survival) were collected from the prospectively collected UZ Leuven LTx database.

Criteria for re-LTx

Re-LTx is performed in carefully selected candidates meeting the same general eligibility criteria as for primary LTx regarding absolute/relative contraindications and risk factors from the consensus statement of selecting LTx candidates by ISHLT in 2021 (Table S1) (9). All cases were discussed at the multidisciplinary team meeting. Moreover, additional requirements are considered when deciding on re-LTx eligibility to reduce risks and ensure a better outcome and survival of patients:

• >2 years post-CLAD onset;
• BOS, rather than RAS;
• Younger patients (<60 years old);
• Ambulatory, rather than hospitalized status;
• Estimated glomerular filtration rate >60 mL/min/1.73 m²;
• No important HLA immunization (unless acceptable virtual PRA and virtual crossmatch possible);
• No non-adherence during postoperative follow-up and adequately treated comorbidities (including gastro-esophageal reflux disease, diabetes mellitus, etc.).

Surgical approach and use of ECLS

During surgery, the patient is placed in a supine position and intubated with a double-lumen tube. Sequential single-LTx is performed via a bilateral anterior thoracotomy (10). Reasons for conversion to clamshell thoracotomy are:

• Preoperative CT scan showing severe fibrotic chest cavity limiting exposure;
• Intraoperative hemodynamic instability requiring maximal hilar exposure.

In the off-pump LTx strategy, ECLS using veno-arterial extracorporeal membrane oxygenation (VA-ECMO) or cardio-pulmonary bypass (CPB) is only considered intraoperatively when there is (11):

• Mechanical ventilatory support failure;
• Pulmonary artery pressure reaching ≥2/3 systolic pressure;
• Hemodynamic instability;
• Bleeding complications.

Central VA-ECMO is the preferred strategy and ECLS is removed after reperfusion.

Statistical analysis

Baseline donor, recipient, and operative variables were compared between patients undergoing re-LTx through sequential anterior thoracotomy without ECLS vs. the more invasive approaches (thoracotomy with ECLS or clamshell with/without ECLS). Continuous variables were expressed as mean ± standard deviation (SD) or median (minimum to maximum) examined with independent-samples t-test (normal distribution) or the Mann-Whitney rank sum test (abnormal distribution), respectively. Pearson’s chi-squared test and Fisher’s exact test were used to analyze categorical variables. All data were analyzed by IBM SPSS version 22.0 for Windows (SPSS IBM, Armonk, NY, USA). P<0.05 was considered statistically significant.

Results

From January 1st, 2007 to December 31st, 2021, 48 re-LTx were performed. One patient with incomplete data, two multi-organ transplants and three single re-LTx were excluded resulting in 42 sequential single (bilateral) re-LTx cases (Figure 1).

Figure 1 Flowchart of the study population. ECLS, extracorporeal life support.

Twenty-six patients (61.9%) received re-LTx by bilateral thoracotomy without ECLS. Sixteen patients (38.1%) had re-LTx through a more invasive approach, among which 14 (eight thoracotomy and six clamshell) were performed with ECLS and two by clamshell approach without ECLS. Donor and recipient pre-operative characteristics are summarized in Tables 1-3.

Emphysema, cystic fibrosis and pulmonary fibrosis were the main indications for their primary LTx. Thirty-eight patients were performed with double-lung Tx, three with heart-lung Tx and one with single-lung Tx. Among all cases, 34 patients underwent their primary LTx through bilateral anterior thoracotomy approach and 28 without ECLS, in total, 26 patients with a full minimally invasive approach. There is no relationship of the use of clamshell or ECLS between the primary and re-LTx (P>0.05, Table 1). FVC% of patients from the bilateral anterior thoracotomy off-pump re-LTx group was higher than patients from the invasive approach group (59.0±22.60 vs. 44.0±16.8 and 34.1±12.3, P=0.004, Table 1). There was no significant difference in indication, FEV1%, 6MWD, ambulatory status, surgical approach and ECLS application between groups during the primary Tx.

For re-LTx, the majority of lungs (33/42; 78.6%) was from donation after brain death (DBD). Cerebrovascular accident (CVA, 21/42; 50.0%) was the most common cause of death. There was no significant difference in donor type, age, gender, cause of death, and PaO₂/FiO₂ between groups (Table 2).

The overall male/female ratio was 22/20. The mean interval between primary and re-LTx was 5.6 years. The indication for re-LTx was mostly BOS (37/42; 88.1%). Patients in the minimally invasive approach group were more at home before the re-LTx (ambulatory) than the invasive approach group (76.9% vs. 25.0%, P=0.001, Table 3). Four re-LTx recipients (9.5%) were sensitized for HLA I (A, B or C) antibody and 13 (31.0%) for HLA II (DP, DM, DO, DQ or DR) antibody at the time of their primary LTx. Twenty-four recipients (57.1%) were HLA antibody sensitized at pre-re-LTx, including 8 for HLA I antibody (19.0%) and 16 for HLA II antibody (38.1%). PRA level >25% was observed in 7 patients (31.8% of 22 tested patients) and the CDC-crossmatch was positive in 6 patients (14.3%). Between groups, there was no significant difference in recipient’s gender, age, the time between primary LTx and re-LTx, BMI, days on the waiting list, indication, FEV1%, FVC%, 6MWD, CMV and EBV status, HLA antibodies sensitization, PRA level >25%, or positive CDC-crossmatch (P>0.05, Table 3).

Among eight clamshell approach subgroup patients, four of them were converted from bilateral anterior thoracotomy intraoperatively for better exposure or bleeding control and four were performed directly by clamshell approach due to small chest, expected adhesions or hemodynamic instability. The operative time of patients undergoing a less invasive approach was significantly shorter than most of the patients with a more invasive approach (471.6±111.2 vs. 704.0±273.4 min, P=0.010). The incidence of PGD-3 at 72-h post-re-LTx was significantly lower in the off-pump clamshell-avoiding group (7.7% vs. 37.5%, P=0.038). In this group, the incidence of PGD-3 within 72-h post-re-LTx (34.6% vs. 68.8%), postoperative mechanical ventilation time (4.8±4.0 vs. 9.1±9.9 days), and ICU stay (14.7±20.8 vs. 27.1±33.8 days) were lower without statistical significance (P>0.05). There was also no statistical difference in postoperative hospital stay (38.7±27.8 vs. 46.4±35.9 days) and need for reoperation within 90 days (38.5% vs. 43.8%). The 1- and 5-year patient survival were similar (less vs. more invasive approach, 88.5% vs. 75.0% and 65.4% vs. 37.5%, respectively, P>0.05). Following re-LTx, DSA was found in 22.5% patients (9 of 40 tested) and 15 patients were diagnosed with CLAD (13 BOS and two RAS) after a mean time of 35 months. The detailed comparison of postoperative characteristics between the off-pump clamshell-avoiding group and the more invasive approach group is shown in Table 4.

One patient from the clamshell group without ECLS died at ICU on the 37th day after re-LTx due to circulatory arrest secondary to hypoxic respiratory failure. One patient was converted from veno-venous ECMO to VA-ECMO intraoperatively and remained on ECMO for 3 days after re-LTx. In one case from the thoracotomy group, intraoperative CPB was needed for making the left atrial anastomosis due to an inadequate patch. This patient died from post-operative bleeding 24 h after the re-LTx.

Discussion

In this retrospective analysis, we observed that in selected cases bilateral re-LTx can be safely performed in a less invasive way by bilateral anterior thoracotomy avoiding both clamshell and use of ECLS. Previous LTx increases the surgical complexity during re-LTx due to adhesions, fibrothorax and limited exposure (12). In these cases, a clamshell approach is generally considered to gain better exposure that allows better vascular control, resulting in reduced anastomotic times (10,12-15). However, a multi-center, retrospective analysis from the LTx working group of the European Society of Thoracic Surgeons analysed 2,690 LTx patients between 2005 and 2020, of which 26 had a previous history of anatomical lung resection by open approach. Survival of these patients seemed comparable to conventional LTx patients, thereby indicating that a history of previous thoracic surgery is not an absolute contraindication (16). In this study, we did not find that the use of clamshell or ECLS during the primary LTx is a prerequisite to use the same approach in re-LTx. Since almost half of the patients who had such invasive approaches in their primary LTx were still able to adopt a less invasive approach in their re-LTx. Therefore, based on our experience, re-LTx can be started through a bilateral anterior thoracotomy.

However, the need for ECLS in (re-)LTx remains a matter of debate. Some centers have shown that routine use of ECLS can result in improved short-term outcome by decreasing the PGD-3 rate at 72 h (17-19). On the other hand, it has also been described that ECLS might result in some vascular and coagulopathy complications such as bleeding and thrombosis (20-23). In our series, we found that re-LTx without ECLS resulted in a PGD-3 rate at 72 h of 7.7% only. In the same cohort, we did not observe much difficulty in weaning from mechanical ventilation and the need for reoperation within 90 days in contrast to the ECLS group. It has previously been described that re-LTx with ECLS resulted in a longer ICU stay and lower overall survival than primary LTx or re-LTx without ECLS (24-26). In our study, patients with ECLS had longer operative time and higher incidence of PGD-3. However, this can be attributed to the fact that ECLS was needed in more complex cases or patients with surgical complications like intraoperative bleeding. Therefore, these two groups cannot be compared head-to-head and the implementation of ECLS in re-LTx should be considered on a case-by-case basis.

Important to stress is that safe clamping of the pulmonary artery is required. Intrapleural dissection of the artery is often difficult and dangerous because of dense adhesions with the bronchial anastomosis and/or its peribronchial fat pad. Therefore, in primary LTx, we suggest not opening the pericardium and performing the anastomosis in the intrapleural space. In re-LTx, we recommend immediately opening the pericardium anterior to the phrenic nerve to encircle the main pulmonary artery intrapericardially between the ascending aorta and the superior cava vein on the right side and medial to the Botalli ligament on the left side. In this sense, during re-LTx, there will be fewer adhesions in the pericardial space where it is easier to clamp the pulmonary artery. If needed, conversion into a clamshell approach with the use of ECLS is always possible. We found that all our RAS patients [and one patient with primary organ failure (POF)] underwent re-LTx with an invasive approach. RAS as a known independent negative prognostic factor is defined by declining pulmonary function and restrictive pulmonary defect without evidence of obstruction following LTx, accounting for 25–35% of all CLAD indications (27-29). In these patients, anatomical changes such as traction bronchiectasis, architectural deformation, volume loss, pleural adhesions and hilar retraction can be observed, which increase surgical complexity (30,31). Furthermore, RAS patients have a higher oxygen requirement and lung allocation score than BOS patients, often resulting in a more urgent Tx (32-35). Therefore, we do not recommend adopting the minimally invasive approach during re-LTx on RAS patients for possible needs of an extended surgical approach and intraoperative ECLS.

We observed that the off-pump clamshell-avoiding group tended to have more male patients. What role gender difference in donor and recipient exerts in LTx and re-LTx is still not well known. Anatomically, the lung capacity and physical reserve in women are usually lower than in men. Gender mismatch could result in organ-chest cavity size mismatch and could be a disadvantage in LTx and re-LTx (36). The female chest cavity is smaller, so a clamshell incision would improve exposure. Moreover, female patients are at higher risk for RAS development, possibly due to more prevalent HLA sensitization in females, which influences re-LTx prognosis as mentioned above (35). However, there are also studies questioning the relationship between gender and (re-)LTx prognosis. Saito et al. (37) did not find any difference in outcomes among BOS- vs. RAS-matched cohorts. Kilic et al. even found male donor to be a risk factor in re-LTx (38). Further research on this gender topic is required in the field of re-LTx.

Recognizing risk factors is crucial when evaluating and selecting the surgical protocol, especially in re-LTx cases. Among re-LTx patients, risk factors include female donor, non-BOS indication (RAS, POF, and others), the time interval between primary and re-LTx <2 years, low BMI, hospitalization before surgery, older age, 6MWD <400 ft, etc. (38-44). We found a similar trend in our study that patients in the less invasive group tended to include more ambulatory status, more BOS indication, fewer female donors, and more days on the waiting list than patients needing a more invasive approach, although some differences were not significant.

Our study suffers from some limitations. The sample size is small due to the rarity of the indication with only 5% being re-LTx in our institution. Moreover, there may have been a selection bias in those patients requiring ECLS and clamshell incision. A multi-center analysis should be conducted on this topic.

Conclusions

In conclusion, our experience showed that off-pump ECLS-avoiding re-LTx is possible and safe in the majority of selected patients and could be considered as a first step during re-LTx.

Acknowledgments

The authors would like to thank all members of the Department of Thoracic Surgery, transplant coordinators, anesthesiologists, intensive care physicians, and pulmonologists involved in the Leuven Lung Transplant Group.

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editor (Ilhan Inci) for the series “Extracorporeal Life Support in Thoracic Surgery” published in Journal of Thoracic Disease. The article has undergone external peer review.

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-64/dss

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-64/coif). The series “Extracorporeal Life Support in Thoracic Surgery” was commissioned by the editorial office without any funding or sponsorship. RV is supported as a senior clinical research fellow by the Research Foundation – Flanders (FWO) Belgium. LJC is supported by a KU Leuven University Chair funded by Medtronic and a post-doctoral grant from the University Hospitals Leuven (KOOR – UZ Leuven). LG received consulting fees from Biotest and Janssen as well as honoraria for lecture from Janssen, support for attending a meeting from MSD and Biotest and participates on advisory board of Janssen. APN received a grant from KU Leuven (C24/18/0730) and support for attending a meeting and speakers fee from Xvivo. The authors have no other 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 Ethics Committee UZ/KU Leuven (No. S51577). There is no experiment in this paper as it is a retrospective study of clinical strategies, therefore informed consent is not required.

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/.

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