Intrathoracic retention time of pericardial fat pads without pedicle in bronchial stump coverage: insights from a retrospective study

Introduction

Bronchopleural fistula (BPF) is a severe complication that arises after anatomical pulmonary resection, such as lobectomy or pneumonectomy. Incidence rates of 5–20% following pneumonectomy and 0.5–5% after lobectomy have been reported (1-3). If BPF develops, the mortality rate is as high as 20–50% (1-4). Commonly reported risk factors for BPF include the site of resection (e.g., right pneumonectomy or right lower lobectomy), prior neoadjuvant therapies (particularly chemoradiation), residual cancer tissue at the bronchial stump, and a history of diabetes or interstitial pneumonia (1-5).

Bronchial stump coverage by autologous tissue is widely recognized as an effective measure for preventing BPF. Several methods have been reported, including the use of pedicled pericardial fat pads, intercostal muscle flaps, pleura, diaphragm, omentum, azygos vein, and pericardium (6,7). Autologous tissue for covering of Bronchial stump is thought to require blood supply, and methods for confirming blood supply using indocyanine green fluorescence or thermography have also been reported (8-10). A randomized study reported pedicled intercostal muscle flaps as useful for covering the bronchial stump to prevent BPF (11). Although reports on other methods have mainly been retrospective studies, no clear answers have been reached on the question of what method is most suitable for covering the bronchial stump to prevent BPF (12). In fact, each method has shown a mixture of advantages and disadvantages. Recently, the use of a free pericardial fat pad (FPFP) without a pedicle has been attracting attention as a method for covering the bronchial stump to prevent BPF (13,14). FPFP has no limitations on reachable range or method of creation, which represent key drawbacks of other methods. The main drawback of FPFP seems to be that the volume decreases over time due to no blood supply (15). However, if the volume of FPFP can be maintained until wound healing of the bronchial stump is sufficiently complete, this method could be considered beneficial for preventing BPF.

The aim of this study was to evaluate the duration the FPFP remains in the thoracic cavity postoperatively and to assess the potential of this method as a strategy for preventing BPF. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-896/rc).

Methods

Patients and methods

Ethics statement

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the institutional review board of Iwate Medical University (No. MH2024-136) and individual consent for this retrospective analysis was waived.

Patient selection

This retrospective cohort study utilized data from the medical records of patients who underwent radical pulmonary resections (excluding segmentectomy, sleeve lobectomy, and salvage lobectomy) in the Department of Thoracic Surgery at Iwate Medical University Hospital between January 2010 and August 2024. Salik et al. explain that if seen within the first 4 postoperative days, BPF is likely secondary to a mechanical failure of bronchial stump closure (16). Therefore, we intended to exclude BPF that developed within 4 postoperative days, but no cases of BPF that developed within 4 postoperative days were found in this study. This resulted in a final sample of 1,745 patients meeting the selection criteria. Of the 1,745 patients, FPFP was used as a covering for the bronchial stump in 59 cases.

Surgical procedures

All operations were performed under general anesthesia. Complete video-assisted thoracic surgery (VATS) lobectomy was conducted via a three-port method under monitoring visualization alone. Hybrid VATS involves a combination of small thoracotomy with direct visualization and monitoring assistance. Cases converted to thoracotomy due to bleeding or severe adhesions were classified as thoracotomy cases.

Bronchial stumps were closed via staplers in all cases. For closure of the bronchial stump, either of two devices was used: a stapler with flat face with equal-height staples or a stapler with stepped face with graduated-height staples. In the case of flat-face staplers, the black or green cartridge was selected. In the case of stepped-face staplers, the black or purple cartridge was selected. Which face and which cartridge to select were left to the discretion of the surgeon. The decision to perform bronchial stump coverage, as well as the choice of technique, was likewise left to the discretion of the operating surgeon. Historically, intercostal muscle flaps have required open thoracotomy, limiting their use to patients on immunosuppressants or dialysis. Since 2016, FPFPs have been utilized and gradually extended to patients with moderate risk factors, such as right lower lobectomy or diabetes.

Upon completing the surgical procedures, sealing tests were performed and additional measures, such as application of polyglycolic acid (PGA) sheets or fibrin glue, were taken in cases showing air leakage. Pericardial fat was collected using an advanced bipolar device, and these were placed at the bronchial stump using fibrin glue and PGA sheets. Finally, chest tubes were placed for postoperative management.

Analysis of residual volume and calculation of residual ratio

The residual volume of the FPFP covering the bronchial stump was assessed via computed tomography (CT). As the initial volume of pericardial fat collected during surgery had not been measured, the volume observed on the first CT taken 1–2 months postoperatively was set as the baseline (100%). No residual fat tissue was observed around the bronchial stump at the time of resection, allowing the fat density near the bronchial closure to be identified as the remaining FPFP.

Among the 59 cases who underwent FPFP, those with first CT conducted later than 2 months postoperatively or with only data from a single CT were excluded, resulting in the analysis of residual volumes from 45 cases. Volume measurements were performed using the 3D Slicer imaging computing platform, free open-source medical image-processing software (version 5.7.0; https://www.slicer.org/, RRID: SCR_005619).

Statistical analysis

All statistical analyses were performed using JMP software (version 14.2.0; SAS Institute, Cary, NC, USA, RRID: SCR_014242). Group comparisons were made via the Mann-Whitney U test or Fisher’s exact test. Logistic regression analysis was conducted, with the receiver operating characteristic (ROC) curve used to determine the cutoff values for variables yielding maximum sensitivity and specificity. Differences between groups were considered significant at the level of P<0.05. Continuous data were expressed as the mean ± standard deviation, and categorical data as number and proportion.

Results

Patients were divided into groups on the basis of the presence or absence of BPF, and group characteristics are summarized in Table 1. Patients who developed BPF were more likely to be older (73.3 vs. 68.7 years, P=0.03) and male (81.0% vs. 59.2%, P=0.04), with low serum albumin levels (4.13 vs. 4.25 g/dL, P=0.048) and performance of right lower lobectomy (57.1% vs. 21.8%, P<0.001) or pneumonectomy (14.3% vs. 2.6%, P=0.001). These findings were consistent with previously reported trends (12-16).

Additional risk factors for BPF identified in this study included clinical N2 status (28.6% vs. 6.6%, P<0.001), prolonged operative time (306.6 vs. 263.9 min, P=0.01), and postoperative pneumonia (33.3% vs. 5.86%, P<0.001).

Residual volumes and ratios of FPFP covering the bronchial stump were measured via the 3D Slicer imaging computing platform (Figure 1). On the basis of the CT performed 1–2 months postoperatively as the baseline, FPFP volume was assessed up to 15 months postoperatively. On average, 7,667 mm³ (range, 4,053–14,124 mm³) of FPFP was harvested. By 2–3 months postoperatively, 84% (±17.7%) of the FPFP volume remained [mean (standard deviation)], falling to 51% (±16.9%) by 3–6 months. Although the overall FPFP volume decreased, the bronchial closure site remained fully covered in all cases at 3–6 months. By 12 months postoperatively, FPFP volume had decreased to 16% (±9.9%), with 2 cases (4.4%) showing no visible FPFP (Figure 2).

Figure 1 Volume measurement of the FPFP using the 3D Slicer imaging computing platform. (A) CT of the left lower lobe bronchus stump. Arrow indicates the stapler, and the area surrounded by the arrowhead shows the density of the fat area. (B,C) The area of the FPFP is indicated in yellow, while areas other than FPFP are green. These are automatically identified by the 3D Slicer imaging computing platform by specifying a number of slices at random, rather than all slices. (D) The mass is recognized as FPFP. The volume of this mass is measured. 3D, three-dimensional; Ao, aorta; Br, bronchus; CT, computed tomography; FPFP, free pericardial fat pad.

Figure 2 FPFP volume change and residual ratio. Changes in the FPFP volume (mm³) (A) and residual ratio (B) for each postoperative period. FPFP, free pericardial fat pad.

The results of multivariate analysis for independent risk factors for BPF are presented in Table 2. Significant factors included serum albumin level <4.1 g/dL [odds ratio (OR) 2.59, P=0.04], right lower lobectomy (OR 4.50, P=0.001), lymph node metastasis (clinical N2) (OR 5.20, P=0.007), and postoperative pneumonia (OR 5.28, P=0.001).

Discussion

This study demonstrated that non-vascularized autologous tissue could retain more than half its volume in the thoracic cavity for approximately 6 months postoperatively. The timing of BPF onset varies, but is commonly reported to occur 10–30 days postoperatively (3,17,18). These results suggest that FPFP may be able to continue covering the bronchial stump until wound healing of the bronchial stump is sufficiently complete. As BPF carries a mortality rate of 20–50%, BPF is one of the most critical complications that surgeons must aim to avoid. Reported risk factors for BPF include the site of resection (right pneumonectomy or right lower lobectomy), residual cancer tissue at the bronchial stump, and a history of diabetes (1-4). Other potential risk factors have also been identified, such as male sex, elevated serum C-reactive protein level, and prior gastrectomy (17). There are reports that the incidence of BPF varies depending on whether a stapler is used and the type of staples used (19). We used stapler for bronchial resection in all cases, and used two types of devices: a stapler with flat face with equal-height staples or a stapler with stepped face with graduated-height staples. Okami et al. reported that although the stepped-face stapler achieved a significantly higher score for staple formation than flat face stapler, no significant difference in the incidence of BPF was seen between faces (20).

To compare whether BPF developed, propensity score matching was performed. There are available in Supplementary file (Appendix 1) and Table S1. The significant differences were observed in the following two items: surgical procedure (right lower lobectomy) and extent of lymph node dissection (ND2a-2). These results suggest that blood flow at the bronchial stump may be a risk factor not only in pneumonectomy but also in lobectomy for BPF developed. However, due to the small sample size, it is not possible to conclusively determine whether covering the bronchial stump is useful for preventing BPF, or whether the above two factors are risk factors for BPF developed, based solely on this study.

Various methods to prevent BPF have been reported, including pedicled pericardial fat pads, intercostal muscle flaps, pleura, diaphragm, omentum, azygos vein, and pericardium. These methods aim to increase vascularity around the bronchial stump using autologous tissue for coverage (6,7,21-23). Pedicled intercostal muscle flaps are considered the most evidence-supported technique (6) but require an incision exceeding 10 cm, which is counter to current trends toward minimally invasive surgery. Pedicled pericardial fat pad or thymus tissue is known as methods that are easily performed under VATS (18). However, the size of the tissues that can be applied is often limited, and coverage may thus be insufficient depending on the location of the bronchial stump. On the other hand, there is report indicating no significant difference in the incidence of BPF between cases where autologous tissue was used to cover the bronchial stump and those where it was not (24). Moreover, it has also been reported that complications due to ectopic ischemia may increase if the autologous tissue is not collected properly (8). These findings highlight that preventive measures for BPF remain undefined.

The use of FPFP has gained attention for its potential to overcome the limitations of other autologous tissues (13,14). Because the FPFP is in a free state with no pedicle, there is no limitation on how far apart the donor and recipient sites can be. Another advantage is that FPFP can be collected in a few minutes under VATS. On the other hand, the lack of a pedicle for FPFP means that the donor tissue cannot obtain blood flow and the volume decreases over time (15). The time and extent of volume decreases of FPFP have not been well reported previously, representing a matter of concern for the effectiveness of this method in preventing BPF.

Free autologous fat pad has been mentioned for cosmetic improvement of facial contours and for augmentation in the treatment of unilateral vocal cord palsy (15,25). Yoshimine et al. reported that the volume decrease for transplanted autologous free fat in rats without a pedicle was due to poor microvascular circulation in the short term and apoptosis in the long term (26). On the other hand, transplanted autologous free fat may be able to survive long term due to revascularization such as that promoted by vascular endothelial growth factor production (10,27). Animal studies in rats and pigs have also demonstrated that free fat pads placed in the thoracic cavity can persist for 10–30 days (26,28). Matsuoka et al. reported that FPFP used for bronchial stump coverage could be observed on CT images for up to 5 months postoperatively, more than sufficient for wound healing at the bronchial stump (13). Similarly, the present study confirmed that more than 50% of the FPFP volume remained at 3–6 months postoperatively, despite some variation. Since BPF commonly develops within one month postoperatively, FPFP coverage may represent a useful and minimally invasive preventive strategy.

Although our study did not find a significant difference in the incidence of BPF between cases with and without bronchial stump coverage, the customary practice of covering bronchial stumps in patients with conditions that delay wound healing (e.g., immunosuppression or dialysis) may have introduced bias.

Prior to 2016, pedicled intercostal muscle flaps were used at our institution, requiring large thoracotomy incisions and 10–15 minutes to harvest, even in experienced hands. As a result, the use of these flaps was limited. Since the adoption of the FPFP in 2016, coverage has become feasible with complete VATS, reducing the harvesting time to approximately 5 minutes. This shift has allowed broader use of the technique, even in moderate-risk cases.

This study showed several limitations that need to be kept in mind. First, the study was retrospective in design and used data from a relatively small number of BPF cases seen at a single institution. Second, the decision to cover the bronchial stump and the choice of method were left to the discretion of the surgeon, introducing potential selection bias. While we cannot definitively state that FPFP is effective for BPF prevention, the finding that more than 50% of non-vascularized autologous tissue remained by 6 months postoperatively is significant. Third, as the volume of the FPFP was not measured at the time of the operation, some shrinkage may have occurred by the time the first postoperative CT was performed. To minimize this error, cases in which first CT was taken 3 or more months postoperatively were excluded from analysis.

The most critical finding was that fat tissue remained over the bronchial closure site at 3–6 months in all cases. Future multi-institutional prospective studies are necessary to address the limitations of this study and identify the most effective and least invasive tissue for bronchial stump coverage.

Conclusions

This study demonstrated that more than 50% of the FPFP volume remained at 3–6 months postoperatively, despite that it was autologous tissue without a pedicle. This significantly exceeded the 1-month postoperative period, which is the peak incidence period for BPF.

Acknowledgments

The authors thank FORTE Science Communications (https://www.forte-science.co.jp/) for English language editing and Professor Yasuhiro Hida of the Department of Thoracic Surgery at Fujita Health University for teaching on how to use the 3D Slicer imaging computing platform.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-896/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-896/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-896/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-2025-896/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 and its subsequent amendments. The study was approved by the institutional review board of Iwate Medical University (No. MH2024-136) 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/.

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