Pulmonary artery reconstruction using cryopreserved allograft for lung cancer: a bi-centric comparative study

Introduction

With advancements in surgical techniques and increased surgeon expertise, combined resection and reconstruction of the pulmonary artery (PA) during lung cancer surgery is now widely accepted as an oncologically established parenchyma-preserving technique. It enables curative surgery while avoiding pneumonectomy when the tumor invades the PA (1,2). However, the incidence of these procedures remains low, with estimates suggesting that PA reconstruction is required in no more than 2% of all lobectomies in thoracic surgery units specialized in conservative procedures (3).

Depending on the extent of PA involvement, reconstruction techniques may include primary closure by direct suture patch closure, end-to-end anastomosis, or conduit interposition. In the latter case, several techniques have been reported in the literature, with various vascular substitutes used for this purpose (4-7). The choice of material depends on the size of the arterial defect and the surgical team’s experience. Although cryopreserved homografts have been used for decades in the reconstruction of congenital heart defects and the replacement of infected prosthetic aortic grafts with excellent results, their use in PA reconstructive surgery for lung cancer remains limited (8,9).

In this study, we sought to present a 20-year experience of PA reconstruction from two tertiary lung surgery centers, with the specific aim of comparing the operative outcomes and mid-term performance of PA grafting using cryopreserved allografts to other techniques, such as patch closure and end-to-end anastomosis. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-869/rc).

Methods

Study design

This study was conducted between January 2001 and December 2021 in two French tertiary centers. Clinical records of all consecutive patients who underwent an arterial sleeve resection for a lung tumor involving the PA were reviewed. The study protocol was reviewed and approved by the Institutional Review Boards of Montpellier University Hospital (IRB-MTP_2021_07_202100888) and Nice University Hospital (IRB-NC 2023 BS 547). The requirement for informed consent was waived because this was a retrospective study involving anonymized patient data. Clinical records of consecutive patients were reviewed retrospectively. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

Patient selection

All patients undergoing arterial sleeve resection for central non-small cell lung cancer (NSCLC) invading PA, during the study dates, were included. Patients undergoing direct PA closure, prosthetic grafting, or bronchial sleeve resection alone were excluded. Patients were then categorized in three different groups depending on the type of PA reconstruction: patch closure, end-to-end anastomosis, or cryopreserved arterial allograft bypass.

Selection and conservation of cryopreserved arterial allograft

The study institution has operated a tissue bank since 1988. Allografts were harvested from brain dead organ donors. Donor serum samples were screened for hepatitis B surface antigen (HBsAg), antibody to hepatitis B surface antigen (HBsAb), hepatitis B core antibody (HBcAb), hepatitis C virus antibody (HCV Ab), human immunodeficiency virus 1/2 antibody (HIV 1/2 Ab), and venereal disease research laboratory (VDRL) for syphilis rapid plasma reagin (RPR). Arterial grafts intended for cryopreservation undergo a stringent sterile processing workflow in a cleanroom environment (ISO7), using an ISO5 laminar flow hood to minimize microbial contamination. Upon opening each Cryokit containing the grafts, microbiological sampling is performed immediately. Specifically, two 5-mL aliquots of the transport solution are aseptically collected into aerobic and anaerobic blood culture bottles, and 1 mL is inoculated into a Schaedler enrichment broth. These samples, labeled with the graft batch number followed by the letter “A” (transport fluid), serve to assess microbial contamination prior to the introduction of the cryoprotectant. After the grafts are transferred into sterile freezing bags and filled with the cryoprotective solution, a second set of microbiological controls is performed: 5 mL of the final preservation fluid is inoculated into new aerobic and anaerobic blood culture bottles, and 1 mL is again placed in Schaedler broth. These are labeled with the same batch number followed by the letter “B” (preservation fluid). No antibiotics are added to either the transport or preservation solutions, ensuring that the results of microbiological testing remain unaffected by bacteriostatic agents. The cryoprotective solution is composed of 70% RPMI-1640 medium (Gibco, Thermo Fisher Scientific, USA), 20% human albumin 4% (40 mg/mL, Vialebex, LFB, France), and 10% dimethyl sulfoxide [dimethyl sulfoxide (DMSO), pure, density 1.1, Sigma-Aldrich, Germany], resulting in a final concentration of 8 mg/mL albumin and 0.11 mg/mL DMSO in the 500 mL solution. This formulation ensures osmotic balance and cellular protection during the freezing process, while maintaining the structural integrity of the arterial tissue. The prepared solution is refrigerated between +2 and +8 ℃ and used within 6 hours of preparation.

Pre operative evaluation

Clinical staging was based on the 8th edition of the tumor-node-metastasis (TNM) system. Preoperative evaluations included bronchoscopy, computed tomography (CT) scans, positron emission tomography-computed tomography (PET-CT), and invasive nodal staging for suspected N2 cases. Neoadjuvant therapy was given to patients with stage IIIA–N2 or higher, followed by mediastinal restaging. Preoperative pulmonary function tests were conducted, and additional whole-body maximal oxygen consumption (VO₂-max test) and Tc-99m perfusion lung scintigraphy were performed when needed.

Surgical procedure

Arterial involvement was attributed either to hilar tumors or lymph node invasion. All patients underwent lung lobectomy with radical mediastinal lymphadenectomy through a posterolateral thoracotomy, under general anesthesia and double-lumen endotracheal intubation. The feasibility of PA sleeve resection was evaluated intraoperatively after achieving proximal and distal vascular control. Following intravenous administration of systemic heparin sodium (0.5 mg/kg), vascular clamps were applied to disease-free segments of the PA. Tumor resection was then carried out en bloc with the involved PA segment, and extended to adjacent structures when necessary. Frozen section analysis was systematically used to confirm negative resection margins. The method of PA reconstruction was chosen after resection, based on the extent of arterial involvement. Three techniques were used: (I) patch angioplasty using either prosthetic (HemaCarotid^®, Maquet^® Gentige Group, Rastatt, Germany) or bovine pericardial patches (XenoSure^®, LeMaitre Vascular, Burlington, USA); (II) end-to-end anastomosis; and (III) bypass reconstruction using cryopreserved allografts (PA or thoracic aorta) when direct reconstruction was not feasible. Vascular suturing was performed using 5-0 or 6-0 polypropylene. At the end of the procedure, the distal clamp was released before finalizing the suture to ensure adequate flushing and proper alignment of the reconstructed vessel (without kinking or torsion). In cases requiring a double-sleeve resection, the bronchial anastomosis was completed first using interrupted 4-0 PDS sutures. Postoperative anticoagulation included subcutaneous administration of 6,000 IU of low-molecular-weight heparin for 15 days.

Data extraction

Data were obtained from patient case notes and electronic medical records and entered into a dedicated anonymized database (Excel, Microsoft Corp, Redmond, WA, USA). The collected data included age, sex, smoking history, comorbidities, pulmonary function tests, whole-body maximal oxygen consumption (VO₂-max test), and Tc-99m perfusion lung scintigraphy when available. Additionally, the following features were recorded: clinical stage, tumor location and size as measured by CT, neoadjuvant therapy modality, histological type, pathological stage, number of lymph nodes and stations removed, type of PA reconstruction, surgical details, duration of chest tube placement, length of hospitalization, need for reoperation, and postoperative complications. Complications included any of the following: adult respiratory distress syndrome (ARDS), pneumonia, atrial fibrillation, prolonged air leak (defined as air leak persistent at 5 days or more, postoperatively), recurrent laryngeal nerve palsy, arterial thrombosis, and bronchopleural fistula. Perioperative mortality was defined as death occurring within 30 days of surgery.

Follow-up

Follow-up data were collected from clinical notes, direct contact with patients and physicians, and the national death registry. Based on routine follow-up protocol, a control CT scan is performed every 6 months for 5 years. When available, pre- and postoperative lung scintigraphy results were recorded for each lobe. Patency of PA reconstruction was assessed using the latest contrast-enhanced thoracic CT. Overall survival (OS) was defined as the time from surgery to death from any cause or the last follow-up, while recurrence-free survival (RFS) was the period from surgery to recurrence or death from any cause.

Statistical analysis

Patient characteristics were described using appropriate descriptive statistics. Outcomes were analyzed using Chi-squared tests or Fisher’s exact tests, while survival outcomes were assessed with Kaplan-Meier analysis, treating death and recurrence as events. When significant differences were found, post hoc analyses with Bonferroni correction were performed to identify specific group differences. Survival and recurrence rates were compared across different types of arterial reconstruction using R software. A significance level of P<0.05 was considered statistically significant. A post hoc power analysis using two-proportion Z-tests was performed in order to detect a substantial risk of type II error in non-significant comparisons. To identify risk factors for recurrence, we performed a logistic regression analysis. As is commonly practiced, variables with a P value <0.2 in univariate analyses were included in the multivariate model. The final model was selected based on the Akaike information criterion (AIC), employing a stepwise backward selection method.

Results

Patient characteristics

A total of 107 patients with centrally located NSCLC underwent lobectomy with PA reconstruction between January 2000 and December 2020. The PA reconstruction techniques included patch closure in 60 patients (Group 1), end-to-end anastomosis in 24 patients (Group 2), and cryopreserved arterial allograft bypass in 23 patients (Group 3). Table S1 summarizes the temporal distribution of surgical groups across the study period. As outlined in Table 1, patient and procedure characteristics were similar across the groups in terms of gender, active smoking status, clinical tumor stage, and neoadjuvant treatment. The rate of concomitant bronchial reconstruction was: 20.0% in Group 1, 41.7% in Group 2, and 52.2% in Group 3. In the pairwise analysis, a difference was observed between group 1 and group 3 only.

Perioperative morbidity and mortality (Table 2)

The 30-day morbidity and mortality rates for the entire cohort were 44.9% and 1.9%, respectively. No significant differences in postoperative complications were observed between the three surgical techniques (P=0.30). Pneumonia emerged as the most common complication, with similar incidence rates across all groups. In Group 1, two patients required decortication surgery for pleural empyema. In Group 2, one patient developed a bronchopleural fistula on postoperative day 15, requiring a completion pneumonectomy, while another underwent reoperation for massive hemoptysis, which resulted in death. In Group 3, one patient required reoperation due to persistent air leak at day 10. Two postoperative deaths occurred in Group 2, while no fatalities were recorded in the other groups (P>0.05).

Patency and perfusion results (Table 3)

The average duration of CT scan follow-up was 21 months (range, 12–93 months). The overall rate of arterial thrombosis in the entire cohort was 1.9%. Two cases of arterial thrombosis occurred in Group 1 (4.1%) and one case in Group 2, while no cases were observed in Group 3. The patency rate among the groups was similar (P=0.77). Regarding perfusion outcomes, the perfusion rate of the remaining lobe was 33.5% in Group 1, 23% in Group 2, and 31.5% in Group 3, with no significant difference between the three techniques (P=0.19).

Oncological outcomes

The mean follow-up period was 32 months. The 5-year OS rate for the study population was 54% [95% confidence interval (CI): 0.38–0.65], and the 5-year RFS rate was 40% (95% CI: 0.30–0.54). No significant differences in OS or RFS were observed between the three groups (Figure 1). As shown in Tables 4,5, the recurrence patterns were consistent across all groups, and multivariable analysis of recurrence identified the following risk factors: pN+ status [hazard ratio (HR) 3.03, 95% CI: 1.25–7.72, P=0.01], squamous cell carcinoma histology (HR 0.45, 95% CI: 0.21–0.97, P=0.044), and adjuvant therapy (HR 3.09, 95% CI: 1.41–6.98, P=0.005) as independent predictors of recurrence. The technique of PA reconstruction was not identified as a risk factor (HR 0.49, 95% CI: 0.18–1.3, P=0.15).

Figure 1 Overall survival and recurrence free-survival curves with (A) the overall survival of the entire cohort, (B) the recurrence-free survival of the entire cohort, (C) the overall survival by reconstruction technique (anastomosis in a red curve, patch closure in a blue curve and cryopreserved allograft in a yellow curve), and (D) the recurrence-free survival by reconstruction technique (similar color pattern). Allog, cryopreserved arterial allograft bypass; Anas, end-to-end anastomosis; Patch, patch closure.

Discussion

The reliability of PA grafting using various prosthetic materials, both synthetic and biological has been confirmed in previous experiences (5,10,11). In this study, we show that PA reconstruction with a cryopreserved allograft results in perioperative complications comparable to patch closure and end-to-end anastomosis techniques. Postoperative mortality, complications, lung perfusion, and locoregional recurrences were similar between groups. The absence of allograft-related complications and the 100% patency rate at 32 months support cryopreserved allografts as a viable option during parenchymal-sparing surgery.

While both synthetic and biological materials can be used, biological materials are generally preferred due to a better biocompatibility and a lower risk of thrombosis (12,13). Autologous pericardium is the most commonly used biological substitute due to its thickness, availability, and cost-free nature. However, it can shrink and curl, leading to lengthening of the reconstructed PA, which may cause vessel kinking, impaired blood flow, and thrombus formation (4,14). The procedure is also time-consuming and carries the risk of cardiac herniation (15), sometimes requiring closure with a bovine pericardial patch or creation of relaxation incision to reduce the missing area by suturing. The use of bovine pericardium for PA grafting may prevent shrinking, however, its suitability remains to be fully established. Regarding the use of the pulmonary vein, it provides a ready-to-use conduit with appropriate stiffness but is limited to cases with tumors not near the pulmonary vein and requiring less than 2 cm of PA resection (16).

The use of cryopreserved allografts for PA replacement was first reported by Berthet et al. in 2013, with a series of 32 PA reconstructions, including 10 with cryopreserved allografts. There were no hospital deaths, and postoperative complications occurred in five patients (9). The results of our study are in agreement with those of Berthet et al. and show similar morbidity and mortality rates to previous reports using other biological materials (5,13,15,17,18), confirming the feasibility and reliability of cryopreserved allografts for parenchymal-sparing surgery. The absence of conduit thrombosis in our study bears consideration, although these results should be interpreted with caution due to the small sample size. One possible explanation could be the preservation of the allograft’s elastic properties and endothelial cells through cryopreservation, which may reduce turbulent flow–induced thrombosis (19). Cryopreserved allografts have also proven superior to fresh allografts due to their stable collagen network (20). In addition, we previously investigated the elastic properties of different biological and synthetic substitute used for PA replacement and showed that human and bovine pericardium, polytetrafluoroethylene (PTFE), and Dacron are significantly less compliant than the PA (21). The bacteriological safety, and the ability of cryopreserved allografts to resist infections are particularly noteworthy. However, their high cost, the logistical resources required for harvesting and preservation, and their limited availability in tissue banks remain important limiting factors to the broader use of cryopreserved allografts.

Previous concerns about using cryopreserved allografts for vascular reconstruction primarily revolved around early and late graft-related complications, such as graft rupture, aneurysm dilation, and pseudoaneurysm formation (22). However, advancements in tissue harvesting, cryoprotectants, freezing methods, and controlled thawing techniques have significantly improved cryopreservation, resulting in decreased complication rates (23). Studies on the long-term performance of homografts in congenital heart surgery have shown a lower risk of conduit replacement or failure with pulmonary homografts compared to bovine and porcine conduits (24). The main risk factors for homograft failure in pediatric patients are conduit sizes <18 mm and younger age (25-27). Considering the average age of lung cancer patients, the risk of late graft-related complications used for PA replacement during parenchymal-sparing surgery is extremely low, if not nonexistent. We have not observed any allograft degeneration during follow-up, though longer monitoring is required.

Arterial patency is paramount in evaluating the success of reconstruction techniques. In this study, with an average follow-up of 32 months, complete patency of the reconstructed PA was consistently achieved across all patients, as confirmed by postoperative CT, with no significant stenosis, aneurysmal degeneration, or calcification. Considering that PA grafting yields results comparable to other reconstruction methods, we believe that arterial replacement is a robust solution. It effectively prevents arterial kinking during PA patch closure and minimizes the risk of excessive tension in an end-to-end anastomosis, particularly in PA resections without combined bronchial sleeve resection. Moreover, this approach ensures the broadest possible resection margins.

Limitations

Our study has several important limitations. First, its retrospective design introduces a potential risk of selection bias, primarily influenced by surgeon preferences and experience. Second, the relatively small sample size limited our ability to conduct more detailed stratified analyses, particularly by tumor stage. Third, although the median follow-up of 32 months is reasonable, it remains insufficient to fully assess the long-term durability of cryopreserved allografts and their potential impact on survival. Fourth, neoadjuvant treatment may result in pathological downstaging, this could potentially confound the interpretation of recurrence risk. Although neoadjuvant therapy was not significantly associated with recurrence in univariate analysis and was therefore excluded from the final multivariate model, this effect should be considered when interpreting pathological staging as a prognostic factor. Fifth, patient-reported outcomes—such as quality of life and functional status—were not assessed. Furthermore, no cost analysis was included, as this study was not designed to assess the economic impact of the technique. However, we acknowledge that the high cost, logistical complexity of harvesting and preservation, and limited availability of cryopreserved allografts remain important considerations for broader implementation. Despite these limitations, our study provides valuable insight into the feasibility and safety of using cryopreserved allografts for PA reconstruction and highlights the need for further studies with longer follow-up.

Conclusions

This study shows that PA reconstruction using cryopreserved allografts is effective and safe in selected patients, Pulmonary perfusion is well preserved, with morbidity and mortality rates comparable to other techniques. The cost and availability of cryopreserved allografts represent the primary constraints limiting their broader use. Late graft-related complications should not represent an additional concern; however, long-term follow-up remains essential.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-869/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-869/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-869/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-869/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 protocol was reviewed and approved by the Institutional Review Boards of Montpellier University Hospital (IRB-MTP_2021_07_202100888) and Nice University Hospital (IRB-NC 2023 BS 547). The requirement for informed consent was waived because this was a retrospective study involving anonymized patient data. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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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