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Eur J Cardiothorac Surg 2006;29:880-885
© 2006 Elsevier Science NL

A new bioabsorbable sleeve for lung staple-line reinforcement (FOREsealTM): report of a three-center phase II clinical trial

Pascal Thomas a , * , Gilbert Massard b , Henri Porte c , Christophe Doddoli a , Xavier Ducrocq b , Massimo Conti c

a Department of Thoracic Surgery, University Hospital of Marseille, France
b Department of Thoracic Surgery, University Hospital of Strasbourg, France
c Department of Thoracic Surgery, University Hospital of Lille, France

Received 4 December 2005; received in revised form 24 January 2006; accepted 26 January 2006.

* Corresponding author. Address: Department of Thoracic Surgery, Ste Marguerite Hospital-CHU Sud, 270 Bd Ste Marguerite, 13274 Marseille Cedex 9, France. Tel.: +33 491 744 680; fax: +33 491 744 590. (Email: Pascal-alexandre.Thomas{at}mail.ap-hm.fr).


   Abstract
Top
 Abstract
1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 References
 
Objective: To investigate on the feasibility, safety, and effectiveness of a new bioabsorbable material for lung staple-line reinforcement. Methods: This prospective open trial included 66 patients (mean age of 56 ± 17 years) who underwent various types of lung resection using staplers with knitted calcium alginate sleeves for buttressing (FOREsealTM, Laboratoires Brothier, Nanterre, France) at three academic centers: 29 lobectomies, 22 emphysema surgeries, 15 wedge resections or lung biopsies. Intraoperative air leakage was assessed at a mean respiratory peak pressure of 30 cmH2O, and rated as grade 1, 2, or 3. Persistent air leakage in the postoperative course, as well as any relevant event, was assessed daily. The follow-up period was of 6 months. Results: No technical problem linked to the device occurred. Hemostasis of the cutting edges was completed in all patients. Fifty-six percent of the patients had no intraoperative air leak and 27.3% had grade 1 leaks. Mean postoperative air leaks and thoracic drainage times were 1.9 ± 2.3 days and 6 ± 5.3 days, respectively. In-hospital mortality was nil. There was no empyema. Mean hospital stay was 9.1 ± 6.6 days. At follow-up, one patient underwent lung transplantation, and pathology of the explanted specimen showed the absence of device-related foreign-body inflammation. One patient complained from metalloptysis, and another one, with a metastatic invasive aspergillosis, developed an infectious recurrence that required reoperation. Conclusions: FOREseal is an ergonomic, safe, and promising new material instead of nonabsorbable materials and xenomaterials for staple-line reinforcement. A randomized comparative study is now in progress.

Key Words: Lung surgery • New technology


   1. Introduction
Top
 Abstract
 1. Introduction
2. Material and methods
 3. Results
 4. Discussion
 References
 
Surgical staplers are widely used for wedge lung resections, to complete the pulmonary fissure during a lobectomy, and for lung remodeling during emphysema surgery. Staplers provide usually reliable hemostasis, but they do not consistently obtain an airtight closure. As a consequence, prolonged air leaks are a common complication of pulmonary surgery that impacts substantially on overall morbidity, hospitalization, and health care costs [1]. Approaches that have been tested in clinical research to diminish the incidence and intensity of pulmonary air leakage include five main categories: fibrin glue [2–4], synthetic polyethylene glycol-based hydrogel sealants without [5–7] or with human serum albumin [8], fleece-bound sealants [9], and staple-line buttressing sheets [10–13]. Reinforcement of the staple lines aims to secure the tissue approximation in compression while applying a uniform longitudinal pressure along the staple rows, thereby avoiding parenchymal tears at lung ventilation and reexpansion. Several materials have been used, including excised parietal pleura, polydioxane ribbon, Teflon felt, bovine pericardium, expanded polytetrafluoroethylene, and collagen patches. Sufficient surfaces of autologous parietal pleura are not always available, and their harvesting may be complicated by a hemothorax and/or dense pleural fusion that is not always desirable, especially in the view of a possible reoperation in the future. Nonabsorbable synthetic materials carry the potential hazard of granulomatous inflammation and/or bacterial colonization, as any foreign body. A potential fear of cross-species transmission of infections cautions against the use of biomaterials originating from animal tissues. These concerns prompted the industry to develop products that were potentially deprived of those risks. The present study was designed to investigate the feasibility, safety, and effectiveness of the use of a new bioabsorbable device to reinforce the staple line during lung surgery.


   2. Material and methods
Top
 Abstract
 1. Introduction
 2. Material and methods
3. Results
 4. Discussion
 References
 
2.1 Study design
This trial was conducted according to the Huriet-Serusclat law of 20 December 1988 regulating the clinical research in France [14]. After approval by the National Commission for the Protection of Human Subjects of Biomedical Research (Marseille – II) on 1st July 2002, 66 patients consented to be enrolled in this open prospective noncomparative trial at three academic institutions (Marseille, 23 patients; Strasbourg, 22 patients; Lille, 21 patients) between September 2002 and March 2003. Inclusion and exclusion criteria were the same in the three centers according to the study protocol. Any patient aged beyond 18 years was considered for inclusion whenever a lung surgery was scheduled. The study was explained to the patient and informed consent was obtained. All patients operated on for emphysema were considered for inclusion, as well as any candidate for a (bi)lobectomy. In the last case, however, patients were also assessed intraoperatively and finally included provided that they presented with incomplete or absent interlobar fissures that needed to be opened anteriorly and/or posteriorly. Candidates for nonanatomic lung resections were those requiring tissue diagnosis or tumor resection while presenting with an emphysematous or interstitial lung disease at CT-scan evaluation.

2.2 Patients
There were 49 males and 17 females whose mean age was 55.8 ± 17 years [range 19–83 years]. The mean body mass index was 23.5 ± 5 kg/m2 [range 15–39 kg/m2]. According to their smoking status, 27 patients were former smokers, 11 were ex-smokers, 14 patients were current smokers, and 14 were nonsmokers. Patients were assigned to three groups according to the surgical procedure: (bi)lobectomy (group 1; n = 29), emphysema surgery (group 2; n = 22), and lung wedge resection (group 3; n = 15). Group 1 patients presented with a primary lung cancer in 24 cases, lung metastases in 3, tuberculosis in 1, and congenital lung anomaly in 1. Operations were as follows: right upper lobectomy (n = 10), upper and middle bilobectomy (n = 1), middle and lower bilobectomy (n = 2), right lower lobectomy (n = 1), left upper lobectomy (n = 9), and left lower lobectomy (n = 6). Group 2 patients underwent pneumoplasty for bullous emphysema in 20 cases, and unilateral lung volume reduction surgery in 2. Group 3 patients underwent a lung wedge resection for tissue diagnosis (n = 3), lung nodule diagnosis (n = 11), and for the resection of a solitary fibrous tumor of the visceral pleura (n = 1). Fifty-three patients were operated on through a lateral (n = 46) or a posterolateral thoracotomy (n = 7), and 13 by VATS. Patients’ characteristics are reported in Table 1 .


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  		Table 1. Patients characteristics
 
2.3 Technique
All operations were performed on a deflated lung by the use of a double lumen endotracheal tube. The following commercially available staplers were used: ETSTM 45 (n = 3) and TLCTM 75 (n = 17) (Ethicon Endosurgery, Johnson & Johnson, Cincinnati, OH, USA), MULTIFIRE ENDO GIATM 60 (n = 25) and GIATM 80 (n = 21) (Autosuture, TYCO, Norwalk, CT, USA). The material used for buttressing was made of polysaccharidic polyglycuronates biopolymers (highly purified fractions from calcium alginates) originating from seaweeds, with documented haemostatic and healing properties. The device consisted of preformed coated knitted bioabsorbable sheets held into the form of sleeves (one cartridge device, one anvil device) sized to fit snugly onto the forks of the surgical stapler (FOREsealTM, Laboratoires Brothier, Nanterre, France). Once fired, the stapler was unlocked and removed. The sleeve was then divided closely to the staple line, the one located on the specimen to be removed, so as to preserve a large strip of material intended to overlap to the lung parenchyma widely beyond both sides of the reinforced staple line. When applied to wet lung surfaces, the material became highly conformable and acquired bioadhesive and sealant properties. All patients received standard double drainage of the chest cavity and the drains were connected to a single-use device with one collecting chamber, water seal and suction control. All patients were extubated in the operative room. Continuous suction was applied at 20–50 cmH2O level, depending on center preferences. When there was no apparent air leakage, a 24 h period test with Heimlich valve was done. Removal of drains was then recommended after chest X-ray control, if the amount of fluid production was less than 200 ml.

2.4 Study endpoints
Hemostasis at the suture line was inspected on the deflated lung before reventilation. All patients, except those operated via a video-assisted approach, underwent a water submersion test with manual lung ventilation at an airway plateau pressure of 30–35 cmH2O. Intensity of air leakage was scored according to a grading system from 0 to 3 (0, no leakage; 1, countable bubbles; 2, stream of bubbles; 3, coalescent bubbles) and recorded. Patients with severe air leakage at one identifiable site underwent further suturing, whenever technically feasible. Air leaks in patients operated through a video-assisted approach were assessed once the trocarts incisions were closed and the chest tubes were in suction. The presence and intensity of air leakage was scored similarly from 0 to 3, according to the air bubbling in the water reservoir, and was monitored on the evening of the first postoperative day, and twice daily thereafter. Incidence and duration of air leaks represented the primary efficacy endpoints. Duration of chest tube drainage as well as in-hospital stay was recorded. Postoperative complications were recorded in all patients. Pneumonia was defined clinically by the occurrence of at least three of the following five criteria: fever, chest infiltrate on radiography, purulent sputum, hypoxemia, and peripheral blood hyperleucocytosis. At follow-up, any clinical or radiological event was checked at routine outpatient visits 1, 3, and 6 months after surgery, and further in patients having experienced potentially device-related complications.


   3. Results
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
4. Discussion
 References
 
3.1 Ease of use
All surgeons noticed that the device quickly and easily loaded onto surgical staplers and stayed on the stapler jaw during tissue manipulation. A short learning period was necessary with video-assisted procedures, due to the absence of a predefined tear line. However, there was no need to conversion in open surgery due to stapler or device malfunction. Mean operative times were 45 min and 89 min after open surgery and video-assisted surgery, respectively. A mean of 2.6 ± 1.5 pairs of sleeves were used.

3.2 Intraoperative hemostasis and air tightness
A perfect hemostasis of the suture line was noted in all cases. The absence of air leak was observed in 37 patients (56%). Grade 1 leaks were noted in 18 patients (27.3%), grade 2 in 9 (13.6%), and grade 3 in 2 (3%). Grade 2 and grade 3 leaks were related in four cases to lung parenchymal tears that became apparent at reventilation. None of these tears involved the reinforced suture line. All were located roughly 1 cm outside the suture line and appeared to be covered by the free edge of the strip. Fig. 1 illustrates these results in each patients group.


Figure 1
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  		Fig. 1. Intraoperative air leaks according to the surgical procedure (group 1: lobectomy; group 2: emphysema surgery; group 3: wedge resections): grade 0: no leakage; grade 1: countable bubbles; grade 2: stream of bubbles; grade 3: coalescent bubbles.

 
3.3 Postoperative air leakage
At 48 h postoperatively, no air leak was present in 55 patients (83.3%): 21/29 group 1 patients, 19/22 group 2 patients, and 15/15 group 3 patients. A grade 1 air leak persisted in seven patients (10.6%: five group 1 and two group 2 patients), a grade 2 in two patients (3%: 1 group 1 & 1 group 2 patients), and a grade 3 in two patients (3%: both from the group 1). Mean duration of air leaks was 1.9 ± 2.3 days [range 0–13 days]: 2.8 ± 2.9 days [range 0–13 days] for group 1 patients, 1.5 ± 1.3 days [range 1–7 days] for group 2 patients, and 0.7 ± 0.9 days [range 1–3 days] for group 3 patients.

3.4 Duration of thoracic drainage and hospitalization stay
Overall mean duration of thoracic drainage was 6 ± 5.3 days [range 2–42 days]: 7.3 ± 7.6 days [range 3–42 days] for group 1 patients, 5.1 ± 0.9 days [range 4–7 days] for group 2 patients, and 4.5 ± 2.4 days [range 3–17 days] for group 3 patients. Respective postoperative hospital stays were 9.1 ± 6.6 days [range 3–51 days] for the whole cohort, 11.4 ± 8.7 days [range 5–51 days] for group 1 patients, 7.9 ± 3.6 days [range 5–21 days] for group 2 patients, and 6.5 ± 3.5 days [range 3–17 days] for group 3 patients.

3.5 In-hospital events
In-hospital mortality was nil. No patient needed reoperation nor blood transfusion. Pneumonia occurred in five patients (7.6%): four group 1 patients, and one group 2 patient. All patients were treated with empirical antibiotic therapy, intensification of physiotherapy, and oxygen supplementation. One group 1 patient required temporary noninvasive mechanical ventilation. Transient episodes of fever (>38 °C) of unknown origin were observed in 13 patients (19.7%): 5 group 1 patients, 6 group 2 patients and 2 group 3 patients. All these events resolved within 72 h either spontaneously (n = 9) or with empirical antibiotics (n = 4). One patient developed a delayed bronchial fistula following a bilobectomy. He was treated conservatively with CT-scan guided chest tube insertion and antibiotics, healed and was discharged at day 51. Another group 1 patient had a wound abscess that necessitated local debridement. There was no empyema. One patient experienced arrhythmia that necessitated pharmacological cardioversion, and a left recurrent nerve palsy as a consequence of extensive lymphadenectomy.

3.6 Follow-up
One patient underwent a double lung transplantation for lung fibrosis, 8 months after a tissue diagnostic lung biopsy. Pleural adhesions were limited to the area in vicinity of the site of the wedge resection. Pathological examination of the operative specimen disclosed the presence of puzzled anhist fibers of alginate, but they lack of any local inflammatory process, especially the absence of multinucleated foreign body giant cells (Fig. 2 ).


Figure 2
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  		Fig. 2. Light photomicrograph of a calcium alginate explant obtained at the occasion of a lung transplantation after 8 months of implantation following reinforced wedge lung resection for tissue diagnosis. Presence of puzzled anhist fibers of alginate. Absence of any local inflammatory process, especially of multinucleated foreign body giant cells. Trichrom haematoxylin–eosin–safran staining (HES) staining, original magnification x200.

 
Five patients died during the study period due to their underlying disease (malignancies in four patients, respiratory insufficiency related to a lung fibrosis in one).

One patient experienced mild hemoptysis and expectorated staples and pieces of the buttressing material 4 months after having undergone unilateral lung volume reduction surgery. Except that, he was well, and benefited greatly from the procedure in terms of pulmonary function and exercise performance. The patient had subsequent recurrences of metalloptysis, but these episodes ceased by 12 months.

Another patient presented with a unique episode of hemoptysis and a round mass at the site of the wedge resection that was attributed to round atelectasis, 4 months after the removal of a post-infectious lung nodule located in the left lower lobe. This immunocompetent patient was known to have this lung nodule since he was operated on for a brain abscess due to Aspergillus fumigatus. At that time, the removal of this lung nodule was decided after a 3-month course of antifungal treatment. Inclusion in the study was motivated by the presence of severe emphysema due to heavy smoking. Initial lung histological findings on the wedge resection specimen were unspecific. Hemoptysis reoccurred and the chest CT-scan showed a growing lung mass (Fig. 3 ). Exploratory surgery was thus decided and a lobectomy was performed 9 months after the initial lung surgery with the fear of a misdiagnosed lung cancer. Pathology showed an inflammatory process with intense polynuclear infiltrates, centered on unabsorbed pieces of alginate, but the absence of multinucleated foreign body giant cells (Fig. 4 ). Microbiological findings included a Candida albicans and a Propionibacterium sp. The patient is now well with a follow-up of 24 months after lobectomy.


Figure 3
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  		Fig. 3. Computed tomographic scan showing a mass in the right lower lobe with calcifications centered within the mass.

 

Figure 4
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  		Fig. 4. Light photomicrograph of a lung pseudotumor due to calcium alginate implantation 9 months earlier at the occasion of a reinforced lung nodule resection. Intense inflammatory process with polynuclear infiltrates, centered on unabsorbed pieces of alginate, but the absence of multinucleated foreign body giant cells. Trichrom haematoxylin–eosin–safran staining (HES) staining, original magnification x400.

 
Other patients had unremarkable clinical and radiological findings at 6-month follow-up.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
References
 
The device proved to be easy to handle and simple to apply both in open and video-assisted surgeries. There was no suture or backing material to remove from the calcium alginate sleeves. Because the device contains no additives or preservatives, no presoaking or rinsing was required as preparatory steps before use.

Biocompatibility must be considered when any prosthetic material is used. Such issue usually has to be extrapolated from animal studies [15]. To the best of our knowledge, there is no available data in the literature dealing with the tissue response in humans to currently used materials for suture line reinforcement. In two patients of the present series, we had the opportunity to assess pathologically the implant site 8 and 9 months after buttressed stapling. In both cases, there were puzzled remnants of calcium alginate fibers without specific cellular inflammation. These findings suggest a minimal foreign-body response, but a degradation process perhaps slower than expected, with the possibility of focal calcifications.

Safety of the device should be addressed as well. One patient experienced a so-called metalloptysis phenomenon. Both staples and buttressing material were present in our patient's expectorate, and this combination is characteristic of almost all seven cases reported to date [16–20]. Of note, all cases of metalloptysis occurred after nonanatomical lung resections and emphysema surgeries, and no cases have been described following other types of pulmonary resection and other conditions. The mechanism of the metalloptysis is unclear. However, it is reasonable to assume that when using the stapler generously during pneumoplasty, relatively large bronchi are traversed by the suture line, and in turn the greater is the number of staple applications, the greater is the risk to encounter this complication, especially in a friable emphysematous lung. Only bovine pericardium has been incriminated to date. Consistently, no cases have been reported involving other inert nonabsorbable material, such as e-PTFE, but metalloptysis is suspected to be an underreported and underdiagnosed complication [19].

It seems that the involved mechanism can also cause a growing mass lesion, as experienced by one patient. Pseudo tumors of the lung after LVRS have been reported previously as an isolated radiological finding, or in association with hemoptysis and/or metalloptysis [21]. Once again, histology did not specifically show foreign body inflammatory changes, but intense polynuclear infiltrates due to multiagent superinfection. It may be hypothesized that special conditions prevailed to the occurrence of this complication in our patient since invasive aspergillus infection, especially central nervous system aspergillosis, is extremely rare in the presence of normal immunity. However, to avoid the use of FOREseal in such a septic setting seems a reasonable recommendation.

To assess the efficacy of the device, we compared our results to those reported for the treated group of available prospective randomized studies having tested the value of fibrin glue, sealant, and various reinforcement materials or topical application human fibrinogen/thrombin-coated collagen patch in similar patient populations. Incidence of air leak after lobectomy at the time of surgery was 60% in the present study, which is in the range of what was observed in the experimental arms of those phase III studies (Table 2 ). Forty-eight hours after surgery, the rate fell at 27.6% in our patients versus 34% in the TachoComb group of the study from Lang et al. [9]. Mean durations of postoperative air leaks, chest tube drainage, and hospital stay were 2.8 days, 7.3 days and 11.4 days, respectively. These values were reported to be ranged from 1.1 days to 5 days, 3.5 days to 6.8 days, and 4.4 days to 9.8 days, respectively. Mean duration of air leaks was 1.5 ± 1.3 days following emphysema surgery and was concordant with that observed after bilateral lung volume reduction surgery (2.5 ± 0.7 days) with the use of bovine pericardium [22]. Finally, air leaks lengthened less than 1 day following lung wedge resection, a value very similar with that observed by Miller et al. [13] after segmentectomy and bovine pericardium reinforcement.


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  		Table 2. Randomized studies of various products for preventing alveolar air leaks in pulmonary resection
 
Cost effectiveness is a more challenging dimension to evaluate. Persistent air leaks are more common in patients with severe emphysema, and when a volumetric inadequacy between the pleural space and the residual lung is expected after surgery. As suggested by our results, preventive actions are likely to be more cost effective following lobectomy and lung volume reduction surgery than wedge resection. To date, four randomized studies have compared buttressed stapling to nonbuttressed stapling, two following lobectomy [11,13] and two following lung volume reduction surgery [10,22]. All dealt with bovine pericardium, and none demonstrated any cost effectiveness benefit. Furthermore, such comparisons should now integrate the adjunct of various strategies that have been proved to be effective in the prevention of persistent air leaks, i.e., creating a pleural tent [23], and early cessation of continuous suction and placing chest tubes to an underwater seal [24]. Furthermore, the management of persistent air leaks should also incorporate provocative chest tube clamping and permissive chest tube removal or patient discharge from the hospital with a chest tube and a Heimlich valve.

To conclude within the limitations of this phase II study, FOREseal appears as an ergonomic, safe and promising new material instead of nonabsorbable materials and xenomaterials for staple-line reinforcement. Whether or not its use in patients undergoing lung resection provides clinical benefits and appears cost effective requires a randomized comparative study, now in progress.


   Acknowledgments
 
This study was supported by a grant from Laboratoires Brothier, Nanterre, France.


   References
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 References
 

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