Significance of staple height on air leak after wedge resection for pulmonary malignant tumor

Introduction

Air leak is the most frequent complication that occurs after pulmonary resection (1). Preventing air leaks is an important task for thoracic surgeons because they lead to a longer chest tube duration and postoperative hospital stay (2,3) and can also be accompanied by major cardiopulmonary complications such as empyema, pneumonia, atelectasis, and arrhythmias (4). In most cases, pulmonary wedge resection is performed using a stapling device (5), but the impact of cartridge selection on occurrence of air leaks has not been clarified. It is estimated that the degree of compression of the lung parenchyma at the stapling site differs depending on which cartridge is used, but the selection of cartridge color generally depends on the surgeon’s preference based on the thickness of the lung parenchyma and the location of the tumor or the presence of underlying lung diseases.

Adverse events in pulmonary wedge resection with stapling devices include air leak, laceration of the visceral pleura, and bleeding, which are caused by a mismatch between staples and tissue thickness; therefore, appropriate selection of the cartridge is important (6). Previous studies have reported that when the pulmonary parenchyma is extremely thin compared to the staple height, compression is insufficient, and air leaks occur (7,8). However, wedge resection for pulmonary malignant tumors generally requires a sufficient margin from the tumor, at least 20 mm or larger than the tumor diameter, which results in the resection of thicker lung parenchyma. We hypothesize that excessive compression of the lung parenchyma by stapling or excessive tension when the lung expands causes air leak due to injury to the visceral pleura around the staple line. In fact, a clinical retrospective study showed that the majority of air leaks were caused by injury to the visceral pleura close to the staple hole or staple line (6,9). Therefore, we consider it is important to use a cartridge with a larger staple height in wedge resection for pulmonary malignant tumors to avoid occurrence of air leaks.

In the present study, we retrospectively assessed the impact of cartridge selection on the occurrence of air leaks after wedge resection for pulmonary malignant tumors with a stapling device using clinical data. In addition, we performed wedge resection on porcine lungs using a stapling device and examined the leak threshold. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1751/rc).

Methods

Patients

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 Yamaguchi University Graduate School of Medicine (No. 2025-090), and individual consent for this retrospective analysis was waived. Patients who underwent thoracoscopic pulmonary wedge resection for pulmonary malignant tumors using Tri-Staple™ (Medtronic, North Haven, CT, USA) from January 2012 to December 2024 at Yamaguchi University Hospital were enrolled in this study. Patients with intrathoracic adhesions, multiple wedge resections, and unknown clinical details were excluded. They were divided into two groups: the black cartridge only group (group B) and the purple cartridge group (alone or in combination with black or camel cartridge). We retrospectively analyzed the clinical data of these patients. Diabetes mellitus was defined based on intake of oral antidiabetic medications or insulin therapy. Interstitial pneumonia (IP) was defined based on computed tomography (CT) images. Pulmonary functions, vital capacity (VC) and forced vital capacity (FVC) and forced expiratory volume in one second (FEV₁) were obtained within one month before surgery. The %VC and %FEV₁ were expressed as the percentage of the predicted value of age, gender, and height. Chronic obstructive pulmonary disease (COPD) was defined by an FEV₁/FVC value of <70%. The percentage of low-attenuation area (%LAA) was defined as LAA/total lung volume, and was calculated using a commercially available imaging software program (AZE, Virtual Place Raijin, Tokyo, Japan) using CT images. The volume of the entire lung area (−600 to −1,024 HU) was defined as the total lung volume, and the volume of the emphysematous lung area (−910 to −1,024 HU) was defined as the LAA. %LAA ≥35% was a significant risk factor for a prolonged air leak, which we have previously reported (10). Tumor size was defined as the total tumor diameter, and total size was defined as the sum of tumor size and tumor depth from the visceral pleura measured based on CT images.

Operation

The operations were performed through two or three port sites (1–3 cm) without rib spreading under general anesthesia with single lung ventilation using a double-lumen endotracheal tube. Wedge resections were performed with either EndoGIA™ Ultra Universal Stapler or Signia™ Stapling System (Medtronic), along with compatible Tri-staple™ or Tri-Staple™ 2.0 cartridges (camel, purple, black) and the length of cartridges were 45 mm. The staple heights of the camel, purple, and black cartridges were 2, 2.5, and 3 mm for the inner row; 3, 3.5, and 4 mm for the middle row; and 4, 4.5, and 5 mm for the outer row, respectively. Wedge resection was performed with a sufficient margin of at least 10 mm from the tumor, if possible, 20 mm or larger than the tumor diameter. After wedge resection, an air leak test was performed using the following method. After filling the pleural cavity with warm sterile saline, the affected lung was re-expanded by bilateral ventilation. It was pressurized until the airway pressure reached 10 cmH₂O, and the presence or absence of air bubbles was confirmed. If an air leak was detected, we performed pneumostasis with polyglycolic acid (PGA) mesh (Neoveil; Gunze, Osaka, Japan) and fibrin glue (Beriplast; CSL Behring, Tokyo, Japan) as described previously (11,12). A 20-Fr chest tube was placed in the thoracic cavity, and the wounds were temporarily closed with adhesive film sheets to obtain an airtight condition. The chest tube was connected to a continuous suction device (MERA Sucuum, Mera Co, Ltd., Tokyo, Japan) and suctioned at –5 cmH₂O. Simultaneously, the lung was inflated by continuous positive pressure at 10 cmH₂O. After confirming that no air leak occurred under these conditions, the wounds were closed, and the operation was completed (13).

Treatment of chest tube

Typically, the chest tube was removed the day after confirmation of no air leak. If the chest tube was removed the day after surgery, the chest tube duration was defined as 1 day. As an exception, if the chest tube was removed on the day of surgery due to pain or for other reasons the duration was defined as 0 days. Chest tube duration was defined as the total number of days for which the chest tube was placed during the hospital stay. If chest tube reinsertion occurred, the number of days after reinsertion was added to the initial number of days. The same postoperative chest drainage protocol was used throughout the study period.

Experimental study with porcine lungs

In this experiment, it was determined that ethical approval for animal experiments was not required because only bronchus and lung blocks were purchased from meat dealers. Six excised porcine lungs from female pigs (6 months old, 100–150 kg) were used. Pulmonary wedge resection was performed using Tri-Staple™ 2.0 45 mm black or Tri-Staple™ 45 mm purple cartridge at the right and left posterior lobes and 4 cm from the bottom (Figure 1A,1B). The lung was submerged in sterile saline and expanded by tracheal intubation with an 8 mm tracheal intubation tube and insufflation. The airway pressure was measured using a cuff manometer connected to the intubation tube (Figure 1C). The pressure at the moment after the bubbles first appeared from the stapling site was defined as the leak threshold (Figure 1D). The upper limit of the pressure measurement was 100 cmH₂O. The right posterior lobe pressure was measured by right one-lung intubation, and then the left posterior lobe pressure was measured in the same manner. The Signia™ Stapling System, along with compatible Tri-Staple™ 2.0 45 mm black and Tri-Staple™ 45 mm purple, was used. Group allocation was performed using block randomization, but the experiment was not blinded. For each specimen, bilateral wedge resections were performed using the allocated color cartridge. The leak threshold was compared with six samples in each group.

Figure 1 Wedge resection using black and purple cartridge in porcine lungs. (A) Porcine lung. Wedge resection was performed in the posterior lobes and 4 cm from the bottom (dotted line). (B) Wedge resection was performed using a purple cartridge. (C) The leak threshold was measured using cuff manometer connected to the intubation tube. (D) Air leak was caused near the stapling site when a purple cartridge was used. The leak threshold was 50 cmH₂O.

Statistical analysis

Fisher’s exact test was used to compare the discrete variables. The Mann-Whitney U test was used to compare the relationships between discrete and continuous variables. Univariate logistic regression analysis was used to determine the relationship between various clinical factors and the occurrence of intraoperative air leaks. The cutoff values for pack-years, tumor size, total size, and number of cartridge use were calculated by Youden index from the receiver operating characteristic (ROC) curves and the area under the ROC curves (AUC). In the propensity score adjustment analysis, a propensity score for the allocation of cartridge color according to preoperative factors [age, gender, body mass index (BMI), pack-years smoked, diabetes mellitus, steroid treatment, IP, %VC, %FEV₁, FEV₁/FVC, %LAA, side, lobe, primary or metastasis, tumor size, total size] was calculated using logistic regression analysis, and the ROC curve and c-statistic were calculated. Multivariate logistic analysis for the occurrence of air leaks was performed with the calculated propensity score and cartridge color as independent variables to evaluate the association between cartridge color and the occurrence of air leaks, adjusted for the propensity score. All P values <0.05 were considered to indicate statistical significance. Statistical analyses were performed using the Stata 16 software program (StataCorp, College Station, TX, USA).

Results

Analysis of clinical data

From January 2012 to December 2024, 286 patients underwent thoracoscopic pulmonary wedge resection for pulmonary malignant tumor at Yamaguchi University Hospital, and Tri-Staple™ cartridge was used in 211 patients. Twenty-eight patients with multiple wedge resections, 36 patients with intrathoracic adhesion, and two patients with unknown details were excluded. As a result, 145 patients were included in the final analysis; of these, 118 patients were in group B, and 27 were in group P. In group P, 20 patients underwent resection with purple cartridge alone, six patients with combined purple and black cartridges, and one patient with combined purple and camel cartridges.

Comparison of patients’ backgrounds and outcomes between the two groups (Table 1) showed that the proportion of patients receiving steroid treatment was higher in group P (P=0.02), and the %VC was lower in group P (P=0.03). There were no significant differences in age, gender, BMI, smoking, pack-years smoked, diabetes mellitus, IP, %FEV₁, FEV₁/FVC, COPD, % LAA, side, lobe, tumor size, and total size. There were no significant differences in operative time and blood loss, or the number of cartridges used for pulmonary wedge resection. In 12 patients (10.1%) of group B and eight patients (29.6%) of group P, air leak was observed during the operation and required pneumostasis with the PGA mesh and fibrin glue, and group B had significantly fewer air leaks (P=0.01). There were no significant differences in chest tube duration between the two groups. Chest tube reinsertion was required in two cases (2.5%) in group B and two cases (7.4%) in group P. One case in group B had IP and the chest tube was removed on 2 days after surgery, but as lung collapse occurred on 7 days after surgery, the chest tube was reinserted. Other cases of chest tube reinsertion, the chest tube was removed on the day of surgery, but chest radiographs revealed collapse of the lung the next day, and the chest tube was reinserted. Ultimately, in all three cases, the air leak was conservatively resolved. There were no cases of complications other than those related to pulmonary fistula such as empyema, pneumonia, atelectasis, and arrhythmias in either group.

According to univariate regression analysis (Table 2), pack-years smoked ≥10 (P=0.02), %LAA ≥35% (P=0.01), lower lobe (P=0.02), tumor size ≥21 mm (P=0.002), total size ≥22 mm (P=0.03), and purple cartridge (P=0.01) may be risk factors for the occurrence of intraoperative air leaks. The cutoff values for pack-years smoked, tumor size, total size and number of cartridge use were calculated to 10, 21, 22, and 4, area under the ROCs were 0.639, 0.581, 0.583, 0.610, respectively.

In the propensity score adjustment analysis (Table 3), purple cartridge may be a risk factor for the occurrence of intraoperative air leaks (P=0.08). The c-statistic for the calculated propensity score was 0.7715, with a 95% confidence interval of 0.678–0.864.

Experimental study with porcine lungs

To evaluate the leak threshold in the porcine lung, pulmonary wedge resection was performed with one cartridge for all specimens. The lung thickness at the time of collapse during resection was 17±1.55 mm (15–18 mm) in the black group and 16±1.55 mm (15–18 mm) in the purple group, with no significant difference. In one specimen in the black group, air leak did not occur under the upper limit pressure of 100 cmH₂O. All air leaks in both groups were caused by injury to the visceral pleura near the stapling site. The leak threshold in the black group was significantly higher than that in the purple group (80.0±16.7 vs. 49.7±22.8 cmH₂O, respectively, P=0.03, Figure 2).

Figure 2 The leak threshold in porcine lungs. The leak threshold of the lungs excised using black cartridges was significantly higher than that of the lungs excised using purple cartridges (80.0±16.7 vs. 49.7±22.8 cmH₂O, P=0.03).

Discussion

Air leaks from the stapling site sometimes occur in cases of pulmonary wedge resection using a stapling device. Surgeons should aim to use cartridges that minimize air leak; however, the impact of cartridge selection on air leak has not been fully validated and different cartridges are used by each facility and surgeon. The results of a large retrospective study of the optimal selection of cartridges for pulmonary stapling showed that the cartridge with the largest staple height at the time were not optimal (14). However, since the examination involved a wide range of diseases and surgical procedures, we examined the selection of cartridges limited to pulmonary wedge resection for pulmonary malignant tumors. In wedge resection for pulmonary malignant tumors, a sufficient margin from the tumor is required, which results in dissection of thicker lung parenchyma (15). We hypothesize that excessive compression of the lung parenchyma by stapling or excessive tension when the lung expands causes air leak due to injury to the visceral pleura around the staple line. Therefore, we consider it important to use a cartridge with a larger staple height to accommodate the increase in tension and avoid air leaks. The results of this study showed that black cartridges should be selected in pulmonary wedge resection for pulmonary malignant tumors. In the present study, intraoperative air leaks occurred in 20 of the 145 cases (13.7%). All air leaks observed in clinical and experimental studies with porcine lungs occurred at staple holes and/or beside the staple line and no air leaks were observed at the stump or staple line overlapping sites. Similar to our results, the location of air leaks in pulmonary resection with a stapling device was the staple holes or the visceral pleura beside the staple line, and no air leaks were observed at the stump or staple line overlapping sites (9). Oozing at the edge of the staple line sometimes occurred, which depends on the degree of tissue compression by the cartridge selection, but no critical bleeding was observed in this study.

In this study, the occurrence of intraoperative air leaks was significantly lower in patients who underwent resection using a black cartridge alone in spite of there being no significant differences in tumor size, tumor depth calculated by adding the distance from the visceral pleura to the tumor size, or emphysematous changes in the lungs. Steroid administration has been reported as a significant risk factor of air leaks after pulmonary resection (16). In the present study, although steroid use was significantly more frequent in the P group, only a few patients developed air leak, and no significant difference was observed in the univariate analysis. Therefore, the influence of steroid use appears to be limited, at least in wedge resection. Propensity score-adjusted analyses suggested that the use of black cartridges may reduce the occurrence of intraoperative air leaks. These results indicate that a black cartridge should be selected for wedge resection for pulmonary malignant tumors. In contrast, no significant difference in chest tube duration was observed between the two groups. This was because we actively performed pneumostasis using the PGA mesh and fibrin glue for cases in which air leak was confirmed during surgery. However, if the occurrence of air leaks can be reduced by using a black cartridge, the use of biological agents can be avoided and the operation time for pneumostasis can be shortened. In addition, black cartridges cost approximately 20 dollars more than camel and purple cartridges, however reducing the occurrence of air leaks can reduce the total cost because avoiding the use of biological agents, the cost of the PGA mesh (10 cm × 5 cm) and fibrin glue is approximately 360 dollars in Japan (13). Despite the short duration of chest tube placement, the average postoperative hospital stay was 6.0 days. The postoperative hospital stay in this study has limited clinical significance, as it is influenced by various social factors such as differences in the healthcare insurance system, geographical factors specific to Yamaguchi University Hospital, and the predominance of elderly patients beyond the patient’s medical condition.

The possible issue of using a cartridge with a larger staple height is the air leak from the edge of the stapling due to insufficient tissue closure. However, no air leak was observed from the edge of the stapling in this study. Moreover, we had no experience of air leaks from the stapling stump when black cartridge was used for division of relatively thin lung parenchyma during anatomical lung resection. Therefore, there would be no concern about insufficient tissue closure using black cartridge for dissecting lung parenchyma.

In the experiment with porcine lungs, it was shown that the black cartridge has a significantly higher-pressure resistance than the purple cartridge. All air leaks occurred because of visceral pleura tearing along the stapling site. There was no difference in the thickness of the lung parenchyma at the caudal 4 cm of the excised posterior lobes. Furthermore, wedge resection was performed with one cartridge, and problems related to the overlapping of staple lines could be excluded. Under these conditions, it was concluded that only the difference in staple height affected the pressure resistance. The pressure resistance values of both cartridges are higher than the normal airway pressure, and it is not clear whether the difference in pressure resistance values itself has clinical significance. However, better pressure resistance is important because higher pressure is expected to be applied to the staple line during tracheal extubation, sputum discharge, and coughing. Although conditions between human and porcine lungs may differ to some extent, this result supports our hypothesis that excessive tension causes air leaks due to injury to the visceral pleura around the staple line when the lung expands. Selecting a cartridge with a larger staple height may reduce the occurrence of air leaks by avoiding this injury. As a result, our clinical and experimental data suggest that routine use of black cartridges in pulmonary wedge resection for pulmonary malignant tumors may contribute to avoiding the occurrence of air leaks from the stapling site.

There were several limitations in our study. First, it was a retrospective study with a small number of cases from a single center. The number of cases and the number of air leaks were so small that statistical analysis by propensity score matching or inverse probability weighting was not possible. The treatment of chest tube was consistent over the study period; however, the use of purple cartridges decreased in the latter half of the study period, making it impossible to rule out the influence of temporal factors or surgeon’s preferences. Furthermore, the mean BMI value of 22.4 was low, and pulmonary function was also favorable, with mean %FEV1 of 99.3% and FEV1/FVC value of 73.7%. It is important to note that patient backgrounds, which vary significantly by country and region, may influence the occurrence of air leak. The condition of lung parenchyma, the location of the tumor, and combination of different color cartridges may have a complex effect on the occurrence of air leaks; therefore, the results of our study should be examined by prospective studies in a multicenter design. Second, this study is limited to Tri-staple™ cartridges. The purpose was to eliminate factors other than the staple height, but comparison using staplers from other companies may also be necessary. Third, this study is only for wedge resection for pulmonary malignant tumors that require a resection margin, and cartridge with a larger staple height may not always be superior for wedge resections for thinner parenchyma such as bulla resection or lung biopsy. Finally, it is difficult to directly demonstrate a correlation between the leak threshold in the porcine experiments and the occurrence of air leaks in clinical practice, and thus the clinical significance of these experiments is limited. Nevertheless, because air leak after pulmonary wedge resection sometimes occurs from pleural injury near the staple line due to excessive compression of the lung parenchyma by staples, the experimental finding that cartridges with larger staple height provide superior leak threshold reinforces the clinical results. This information may serve as a useful reference for thoracic surgeons when selecting cartridges for pulmonary wedge resection.

Conclusions

Our clinical and experimental data suggest that selecting the black cartridge is better than the purple cartridge in avoiding the occurrence of air leak after pulmonary wedge resection for pulmonary malignant tumors.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1751/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1751/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1751/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-2025-1751/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 Yamaguchi University Graduate School of Medicine (No. 2025-090), 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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