Ann Thorac Surg 2005;80:2321-2324
© 2005 The Society of Thoracic Surgeons
New technology
Free Pericardial Fat Pads Can Act as Sealant for Preventing Alveolar Air Leaks
Isao Matsumoto, MD
*
,
Yasuhiko Ohta, MD,
Makoto Oda, MD,
Yoshio Tsunezuka, MD,
Masaya Tamura, MD,
Kazuyuki Kawakami, MD,
Go Watanabe, MD
Department of General and Cardiothoracic Surgery, Kanazawa University, Kanazawa, Japan
Accepted for publication April 25, 2005.
* Address correspondence to Dr Matsumoto, Department of General and Cardiothoracic Surgery, Kanazawa University, Takara-machi 13-1, Kanazawa, 920-8641 Japan (Email: mat{at}p2223.nsk.ne.jp).
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Abstract
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PURPOSE: This study was performed to investigate the safety and efficacy of a method using free pericardial fat pads as a sealant to prevent intraoperative and postoperative alveolar air leaks.
DESCRIPTION: Animal experiments were performed. After pulmonary parenchymal defects were created in 4 dogs, the alveolar air leaks were sealed with free pericardial fat pads. Clinical application was applied in 23 patients who underwent pulmonary resection, air leaks with stream of bubbles, or worse, were sealed with free pericardial fat pads.
EVALUATION: All dogs survived for 1 month without complications. At sacrifice, all treated lungs had expanded adequately and the implanted fats remained on the lung surface. Histologic examination showed that the excised edge of the lung was closed with granulation. The clinical outcome showed the mean duration of air leaks, chest drain, and postoperative hospitalization were 2.3 ± 3.1 days, 4.3 ± 3.2 days, and 11.1 ± 3.7 days, respectively. Recurrent air leaks were not observed after removal of the chest tube. No adverse effects were observed after surgery.
CONCLUSIONS: The use of free pericardial fat pads was able to successfully prevent alveolar air leaks.
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Technology
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In patients undergoing pulmonary resection, alveolar air leaks (AAL) frequently develop at areas of dissection or along lines of parenchymal closure using sutures or staples. Prolonged air leaks occasionally induce complications, such as empyema [1], and hinder early postoperative removal of chest tubes, early recovery, and early discharge. Thus, prevention of air leaks is an important goal in managing patients after pulmonary resection. In order to prevent air leaks, it is necessary to protect the residual lung during pulmonary resection. However, in cases with emphysematous change or incomplete lobulation, air leaks occur despite techniques to minimize them, such as the use of sealant agents or bovine pericardial strips [2–8]. As an alternative, a closure method using the patient's own biological tissues, such as free pericardial fat pads (FPFP), has been adopted to seal AAL at our institution. Prior to the clinical study, we investigated the effects of FPFP using a canine model. Based on the results of this animal study, we investigated the safety and efficacy of this method to reduce AAL after pulmonary resection in clinical settings.
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Technique
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We confirmed the effects of FPFP in preventing AAL after pulmonary resection with an animal experiment in 4 adult beagle dogs (average weight, 10.8 kg). Humane care was provided for all dogs in accordance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH Publication No. 86-23, revised 1985). Dogs were pre-medicated and anesthetized using atropine sulfate (0.02 mg/kg) and ketamine hydrochloride (10 mg/kg). The dogs were intubated and mechanically ventilated. The anesthesia was maintained with 1% isoflurane plus 50% nitrous oxide gas and 50% oxygen. A right posterolateral skin incision was made, and a thoracotomy was performed. First a 2 x 2 cm pulmonary parenchymal defect was created (Fig 1A). Next the FPFP were harvested to cover the defect. The air leaks were sealed with the following procedure. Free pericardial fat pads were sutured to the lung with 4-0 PDS II (Ethicon, Somerville, NJ) (Fig. 1B). At this juncture, the excised edge of the lung was closed using the horizontal mattress closure method and the fat mass was applied by pressing and implanting it onto the area of the air leaks. The needle was passed through the FPFP first without piercing the lung directly, facilitating reinforcement at the needle site. After an absence of air leaks was confirmed by an air leak test at an intra-airway pressure of 30 cm H2O, a chest tube was inserted. The chest tube was removed after chest closure. Antibiotics were administered before and after the operation. The dogs were sacrificed 1 month after surgery, and the treated lungs were examined by histologic examination.
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Fig 1. (A) A 2 x 2 cm pulmonary parenchymal defect was created. (B) Air leaks were sealed with free pericardial fat mass.
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Clinical Experience
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Among 146 consecutive patients with lung tumors who underwent pulmonary resection between August 2003 and July 2004, FPFP were used to seal AAL in 23 patients. After pulmonary resection was completed, air leaks were identified by inflating to 15 to 25 cm H2O pressure. In order to assess the degree of air leak, we used a semiquantitative scale according to Wain and colleagues [2] as follows: grade 0 = no leaks; 1 = countable bubbles; 2 = stream of bubbles; 3 = coalesced bubbles. When air leaks from pulmonary parenchyma appeared to be grade 2 or worse, the required amount of FPFP were harvested to cover the area of the air leaks using the Harmonic Scalpel (Ethicon Endo-Surgery, Cincinnati, OH). We did not use this technique for grade 1, because air leaks may cease in time without requiring sealant agents. The air leaks were sealed with the same method used in the experimental study. After application of FPFP to each identified air leak, a second leak test was performed. All patients had one or two chest tubes placed apically. Cephalosporin antibiotics were administered before and after surgery. Other sealants were not used during this period. Chest tubes were placed postoperatively under negative pressure suction of 10 cm H2O for 24 hours, and were later placed in water seals. Chest tubes were removed after the air leaks disappeared, and lung expansion was evaluated by chest roentgenogram and when drainage was less than 150 mL per 24 hours.
Assessment of Sealing Using FPFP
Data were collected on age, gender, pulmonary pathology, type of surgery, preoperative forced expiratory volume in 1 second per forced vital capacity ratio, duration of air leaks and chest tube drainage, length of hospital stay, and postoperative complications. In order to assess the degree of postoperative air leaks, we used the same grading as for intraoperative air leaks. Chest roentgenograms were obtained within 6 hours of surgery, once everyday until the day after the chest tube removal, at discharge, and at the 1-month follow-up examination. After chest tube removal, all patients were monitored for clinical evidence of a pneumothorax or empyema. All treated patients underwent clinical examination and chest computed tomographic scan between 3 and 6 months after surgery.
Results
Animal experiment
When the chest tube was removed after chest closure, there were no air leaks. All dogs survived for 1 month without complications. At sacrifice, empyema was not observed. Areas where FPFP were applied were mildly adherent to the chest wall. All treated lungs had adequately expanded. In all dogs, the fat remained on the lung surface (Figs 2A, 2B). Histologic examination showed that the excised edge of the lung was closed with a layer of granulation, which formed between the excised edge of the lung and the fat mass (Fig 3A). The fat structure was maintained, although the feeding vessel to the fat mass could not be identified (Fig 3B).
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Fig 2. (A) Lung specimen. (B) Histological findings (hematoxylin and eosin stain). The fat mass (arrow) remained on the lung surface.
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Fig 3. (A) The excised edge of the lung was closed with granulation. (B) The implanted fat structure was maintained (*granulation layer; A and B: hematoxylin and eosin stain).
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Clinical outcome
The characteristics of the 23 patients are demonstrated in Table 1. Pathologically, 20 patients had primary lung cancer, and 3 patients had metastatic lung tumor (laryngeal cancer [1 patient], breast cancer [1], and malignant fibrous histiocytoma [1]). The number of inserted chest tubes was 1 in 5 patients and 2 in 18 patients. Two patients suffered from severe emphysema with forced expiratory volume in 1 second per forced vital capacity of less than 50%.
The mean time of harvesting the FPFP was 4.4 ± 0.7 minutes. Most of the air leaks we treated resulted from dissection of the fissures between the lungs. All the patients in whom we used FPFP, the air leaks were sealed at the time of chest closure. After returning to their rooms, 12 patients were grade 0 and 11 patients were grade 1. On the day after surgery, 13 patients were grade 0, 7 patients were grade 1, 2 patients were grade 2, and 1 patient was grade 3. On the fifth postoperative day, 1 patient was grade 1, another was grade 2, and all other patients were chest tube free. The mean duration of air leaks and chest tube insertion was 2.3 ± 3.1 days (range, 0 to 12 days) and 4.3 ± 3.2 days (range, 1 to 13 days), respectively. Recurrent air leaks were not seen after chest tube removal, and postoperative hospitalization was 11.1 ± 3.7 days (range, 7 to 21 days). No trace of the fat mass drained out postoperatively, and no adverse effects, such as empyema or bleeding were observed after surgery. There were no obvious adverse trends concerning fever, amount of secretion from chest tubes, and the general condition of the patients. Follow-up computed tomography was performed on all patients, but no fat masses were identified.
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Comment
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Prolonged air leaks occasionally induce complications and may require further intervention, including placement of additional chest tubes, chemical pleurodesis, and further surgery. To prevent these air leaks, various sealants are used. Although the application of fibrin-based sealants is reported to reduce AAL experimentally [3], clinically, their efficacy in reducing postoperative air leaks is questionable [2, 4–7]. In addition, the sealant is very costly and carries a small risk of infection by viruses such as human parvovirus B19 [9]. As an alternative, several studies have examined new synthetic tissue sealants for AAL. However, polyethylene-glycol-based products may trap bacteria and lead to a higher incidence of empyema [2, 6, 7]. The effectiveness of a new biodegradable polymeric sealant was recently demonstrated [7], and although this sealant is safer and more effective than other sealants, at present, there are no perfect sealants. The ideal sealant to stop AAL should be easy to apply and adhere sufficiently to withstand the pressure of forceful coughing while allowing the lung to expand. The material must be nontoxic and inexpensive. In addition, we believe that it is preferable to use the patient's own biological tissue. Yoshimura and colleagues [8] showed that gluing a pedicled pericardial fat pad onto the surface of a leaking raw lung using fibrin glue reduced AAL after pulmonary resection. However, areas where pericardial fat pads can be used are limited by pedicle length. Therefore, we selected FPFP. We believe that no previous study has used FPFP to prevent AAL.
Based on histologic findings in animal experiments, we believe the mechanism of air leak closure to be as follows: Initially, air leaks are closed physically by the fat mass. The implanted fat mass may be nurtured by new blood vessels from the pulmonary parenchyma. Concurrently, wound healing would begin and facilitate granulation between the excised edge of the lung and the fat mass. Clinically, although chest computed tomographic scans during postoperative follow-up failed to confirm the fat mass, no traces of the fat masses were drained postoperatively. Based on the results of the animal study, although dogs with healthy lungs were selected, it is highly possible that the implanted mass remained even in the damaged human lungs.
Several advantages can be cited in relation to the use of FPFP. There is no risk of the infectious complications associated with fibrin-based sealant, the present method is quite inexpensive, and the required amount of material is accessible in the surgical field and thus takes less time. Clinically, when compared with the results for other reported methods of sealing AAL, our results were in no way found to be inferior [2, 4–8], although study design differed in each study. Our technique could be easily performed and no complications occurred postoperatively. We believe that the use of FPFP is practical and effective for preventing intraoperative and postoperative air leaks during pulmonary resection. On the other hand, our method was not effective in some cases. Although this technique was able to seal most intraoperative AAL, 43% of our patients experienced recurrence of air leaks, although the majority of these air leaks were grade 1. The cause of leak recurrence may be tearing of the sutured sites by the effects of coughing. The key to overcoming this effect is suturing with light tension but not overly tight closure. Some training would thus be required and there may be a learning curve. In addition, the implanted fat mass may become atrophic on the emphysematous lung because the emphysematous lung has a poor blood supply within its tissues. However, we believe air leaks will cease by granulation before the fat mass becomes atrophic. In order to clearly establish the effects of FPFP, a randomized trial with a greater number of patients to prospectively compare a group using FPFP with a group using another sealant or nothing will be needed.
In conclusion, the use of FPFP was able to successfully prevent intraoperative and postoperative AAL. This novel technique can be an optional method and an alternative to some sealant agents for sealing air leaks.
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Disclosures and Freedom of Investigation
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The authors of this article had full control of the design of the study, methods used, outcome indicators, analysis of data, and production of this report. We also had no financial relationship with Ethicon and Ethicon Endo-Surgery, nor any other companies or institutes.
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Footnotes
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Disclaimer The Society of Thoracic Surgeons, the Southern Thoracic Surgical Association, and The Annals of Thoracic Surgery neither endorse nor discourage use of the new technology described in this article.
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References
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P. Goldstraw
Invited commentary
Ann. Thorac. Surg.,
December 1, 2005;
80(6):
2324 - 2325.
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