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Eur J Cardiothorac Surg 2004;25:160-166
© 2004 Elsevier Science NL

Efficacy and safety of topical application of human fibrinogen/thrombin-coated collagen patch (TachoComb) for treatment of air leakage after standard lobectomy

^a Department of Cardiothoracic Surgery, University of Vienna, Währinger Gürtel 18-20, Vienna A-1090, Austria
^b Thoracic Surgery Clinic, Korányi National Institute for Pulmonology, Budapest, Hungary
^c Ruhrland Clinic, Essen, Germany
^d Central Clinic, Augsburg, Germany
^e University Hospital, Uppsala, Sweden

Received 8 August 2003; received in revised form 11 November 2003; accepted 16 November 2003.

^* Corresponding author. Tel.: +43-1-40-400-5644; fax: +43-1-40-400-5642
e-mail: walter.klepetko{at}akh-wien.ac.at

	Abstract

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

 
Objective: Persisting air leakage after pulmonary resection remains a significant problem. The aim of the study was to evaluate the incidence of air leakage after standard lobectomy and test the efficacy and safety of TachoComb (TC). Methods: A total of 189 patients undergoing lobectomy were enrolled in a multi-centre, open, randomised, and prospective study to test the efficacy and safety of TachoComb (TC) for air leakage treatment. Air leakage was assessed by water submersion test, and scored as grades 0 if no, 1 if countable, 2 if a stream of and 3 if coalescent bubbles have been observed. Any sites with grade 3 air leakage received further stapling or limited suturing until grade 0, 1 or 2 was obtained. Treatment of air leakage was done with TC or suturing according to randomisation. Air leakage was assessed by further submersion tests. Postoperative air leakage was assessed using the Pleur-Evac system. Results: Overall incidence of air leakage 48±6 h after surgery was 34% for TC and 37% for standard treatment (P=0.76). The reduction of intra-operative air leak intensity in the subgroup with grades 1–2 was significantly higher for the TC group (P=0.015). Postoperative air leakage intensity in the subgroup with air leakage grades 1–2 was lower for TC than standard treatment (P=0.047). The mean duration of postoperative air leakage in the subgroup with grades 1–2 was shorter for the TC group than for standard treatment, i.e. 1.9±1.4 vs. 2.7±2.2 days (P=0.015). Conclusions: TC could be proven as well-tolerated and safe. In the subgroup of patients with established air leakage, TC showed superior potential in reduction of intra-operative air leakage as well as in reduction of intensity and duration of postoperative air leakage.

Key Words: Air leakage • Lung tissue sealing • TachoComb

	1. Introduction

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

 
Persisting air leakage after pulmonary surgery may have negative consequences on overall morbidity, hospitalisation and health care costs.

Air tight closure of the lung parenchyma after pulmonary resection is therefore a factor of major importance. However so far the incidence and intensity of air leakage after standard lobectomy has not been systematically evaluated within prospective clinical trials.

The standard method for treatment of air leaks after lung resection represents surgical suturing or stapling. Other approaches have been tested in clinical routine, such as fibrin glue [1–6], synthetic polyethylene glycol-based hydrogel sealants [7–9], as well as fleece-bound sealants [10–12] or staple line reinforcements [13–17]. However, the efficacy and safety of the newest generation of fleece-bound sealants, which includes human components only (TachoComb, TC) remains unproven.

The present study was therefore performed to evaluate

1. the incidence of air leakage after standard lobectomy for lung cancer patients,
   
2. the safety of the use of a new fleece-bound fibrin glue sealant (TC), and
   
3. the efficacy of this device for prevention and treatment of air leakage after standard lobectomy.
   

The trial was conducted according to the ethical principles of the Declaration of Helsinki [18], in accordance with local requirements and with Good Clinical Practice [19].

	2. Materials and methods

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

 
2.1. Study design
The trial was set up in a randomised prospective parallel group design and was conducted at five different high-volume thoracic surgery centres in four countries, Vienna, Austria (52 patients), Budapest, Hungary (65 patients), Essen, Germany (44 patients), Augsburg, Germany (16 patients) and Uppsala, Sweden (12 patients). The trial was open since the appearance of TC made it impossible to blind the two test treatment arms. The trial population consisted of lung cancer patients undergoing elective standard lobectomy with or without mediastinal lymphadenectomy. Main inclusion and exclusion criteria are summarised in Table 1.

Standard lobectomy was performed through antero-lateral or postero-lateral thoracotomy according to the centres' preference. Division of the parenchymal bridges and closure of the bronchial stump were uniformly performed with commercially available stapling devices. The parenchymal resection sites and the stapling lines were further handled with the use of electrocautery or single stitch 4.0 sutures when regarded as necessary by the surgeon. Thereafter all patients underwent a water submersion test with lung inflation pressure of 20–25 cmH₂O and intensity of air leakage was scored according to a grading system from 0 to 3 (0, no leakage; 1, single countable bubbles; 2, stream of bubbles; 3, coalescent bubbles). The anaesthetist was asked two close the APL valve, switch to manual ventilation and maintain an airway plateau pressure between 20 and 25 cmH₂O. Severity was taken from the site with the highest grade if there were more than one site. Patients with air leakage degree 3 underwent further suturing or stapling until the intensity of the air leakage was reduced to degree 2.

Thereafter patients were stratified in a group with air leakage grade 0 and a group with air leakage 1–2 and were randomised to treatment with TC or further standard surgical treatment.

2.2. TachoComb group
For management of air leakage sites, TC was applied under aseptic conditions to all parenchymal resection area(s). TC is a sterile ready-to-use absorbable patch consisting of an equine-collagen fleece coated with human fibrinogen and human thrombin. When applied to wet tissue surfaces, the coagulation factors dissolve and form a stable fibrin clot which tightly glues the collagen fleece to the tissue surface. The patch size is 9.5x4.8x0.5 cm³. If more than one patch was needed, the individual patches had to overlap at least 1 cm beyond the immediate margins.

2.3. Standard surgical group
For air leakage management in the control group, single or continuous running sutures of 4/0 PDS or Vicryl were used according to the routine of the centre.

Thereafter all patients underwent a second water submersion test and the degree of air leakage was recorded again and compared to the pretreatment test. All patients received standard double drainage of the chest cavity and the drains were connected to a Pleur-Evac system (Pleur-Evac^® A-6000 or A-6002 from Deknatel Snowden Pencer). This single-use-device consists of a three-bottle-system with collecting chamber, water seal and suction control. Continuous suction limited with 10–15 cmH₂O was applied. The Pleur-Evac system allows one to determine the relative intensity of air leakage by air bubbles appearing in the water reservoir. The extent of migration of these bubbles was measured on a scale from 0 to 7 units. 0 means absence of air bubbles, 1 means a very minor air leakage whereas 7 means the most intensive air leakage. The device is used routinely in many hospitals and provides a standard in the assessment of air leakage. Although the scale is only semi-quantitative, the observations of the individual course of air leakage as well as inter-patient comparisons are possible.

The presence and intensity of air leakage was monitored on the morning of the first postoperative day and every 24 h thereafter. If there was no apparent air leakage at rest, additional provocation by coughing was performed. Removal of drains was recommended 24 h after the first observed absence of air leakage, if the amount of fluid production was <200 ml. However, since the duration of the thoracic drainage is a parameter of high variability, it was not considered as a parameter of investigation.

2.4. Study endpoints and statistics
The primary efficacy endpoint of the study was incidence of air leakage 48 h after lobectomy with a time frame of ±6 h; this time frame (42–54 h) will be referred to as 48 h in this report. Secondary efficacy endpoints were reduction of intra-operative air leakage intensity after the first test treatment, as well as intensity and duration of postoperative air leakage up to postoperative day 9.

Postoperative mortality and morbidity pattern was recorded in all patients until a final follow-up control 1 month postoperatively.

The statistical methods used for the efficacy analyses were: Fisher's exact test for incidence of air leakage at 48 h, Mann–Whitney test for reduction of intra-operative and intensity of postoperative air leakage, and log-rank test for duration of postoperative air leakage, respectively. A level 0.05 was considered to be significant.

All statistical analyses were performed for the whole cohort of patients (air leakage grades 0, 1 and 2 at second submersion test) and for the subgroup of patients with established air leakage grades 1 and 2 only.

	3. Results

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

 
3.1. General results
A total of 217 patients were screened preoperatively and 189 fulfilled the inclusion criteria after lobectomy and entered the study, among whom 96 were randomised to the TC group and 93 to the standard surgical group. The number of patients who completed the study was 186 and the remaining three were discontinued due to non-compliance with the protocol. One patient of the TC group was discontinued after pulmonary embolism, in one patient from the standard group a different drainage device was used and in a second case the resected specimen proved to be not a primary lung cancer, but a gastrointestinal metastasis.

Of the 189 patients, 124 (66%) were male and 65 (34%) female. Mean age was 61.1±10.3 years and mean weight 75.7±14.3 kg. All patients were caucasian, 90 patients (48%) were smokers and 40 patients (21%) regularly consumed alcohol. Both groups were comparable with regard to demographic and baseline variables (Table 2).

Surgical variables are summarised in Table 3.

View larger version (28K): [in this window] [in a new window]   Fig. 1. Incidence of air leak after lobectomy in all patients and 48 h after surgery (TC and standard group). P=0.76, odds ratio=0.91, CI 0.48–1.72.

View larger version (28K): [in this window] [in a new window]   Fig. 2. Intra-operative air leak intensity after test treatments. P<0.015.

For patients with grades 1–2 air leak at time of randomisation, air leakage was present in 39% in the TC group and 49% in the standard surgical group, respectively (P=0.29; odds ratio, 0.61; 95% CI, 0.24–1.56).

3.5. Intensity of postoperative air leakage
Postoperative air leakage intensity, assessed by grading at the Pleur-Evac device, was expressed as area under the curve (AUC) of the daily recordings. The mean AUC of the recordings was 0.77±1.72 (range 0–9) for TC group and 1.27±2.76 (range 0–15) for standard treatment group. The estimated treatment difference was -0.56 in favour of TC group (CI, -1.17 to 0.05, P=0.07).

Analysis of the subgroup of patients with established air leakage grades 1–2 revealed a mean AUC of 1.04±1.79 (range 0–8) in the TC group versus 2.1±3.42 (range 0–15) in the standard treatment group (P=0.047; Fig. 3) .

View larger version (26K): [in this window] [in a new window]   Fig. 3. Postoperative air leak intensity expressed by mean area under the curve of the daily recordings.

View larger version (28K): [in this window] [in a new window]   Fig. 4. Mean duration of postoperative air leakage.

	4. Discussion

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

Although the routine use of surgical staplers for division of parenchymal areas has improved the primary sealing of resection lines itself, a number of potential sources for air leakage do remain. Especially the hilar region after lobectomy, stitch holes after suturing, as well as other lacerated or decorticated lung surface areas are among them. Even when complete airtight sealing is achieved at the end of an operation, air leaks can develop at any point of time during the postoperative course. Deriving from there, a need for an effective tool for prevention of lately developing air leaks is given.

This study was therefore designed to evaluate both the therapeutic potential of a fleece-bound sealant for treatment of established air leaks, as well as the prophylactic value for prevention of its later appearance. The inclusion of all patients with and without air leak was clearly different from other studies [6,8], where only patients with pronounced leaks were investigated. This allowed one to analyse the incidence of observed air leaks after standard lobectomy, which was surprisingly low with only 48%. Limited information about this parameter exists mainly from one multi-centre trial with 172 patients, where Wain et al. [9] had observed a 70% incidence after different types of lung resection, including single and multiple wedge resections. We believe that this lower incidence was partly due to the severe exclusion criteria, since air leakage due to adhaesiolysis was excluded.

Standard therapy of remaining air leakage after pulmonary resections consists of suturing with or without pledges, use of electrocautery and in some situations of repeated stapling [21]. Buttressing the staple line has been recommended to overcome this problem, but this therapy can only be used in a prophylactic setting [13–17]. Beyond that, different fibrin glue products [1–5,20], synthetic, polyethylene glycol-based, bioresorbable hydrogel sealants [6–9], as well as fleece-bound sealants [10–12] have been tested in selected and non-selected patient series.

TC, developed to achieve a haemostatic and tissue sealant effect, consists of an equine collagen patch carrying the fibrin glue components human fibrinogen and human thrombin. Since it contains no bovine components, the risk of transmitting diseases such as bovine spongiform encephalopathy (BSE) has been eliminated.

It is basically a sterile ready-to-use absorbable patch that can be applied after premoistening with physiological saline by pressing it to tissue surfaces. This simple handling represents an advantage to the use of synthetic hydrogel sealants, which need a sophisticated application procedure including mixing or warming up of primer and sealant solutions, and photopolymerisation with xenon light [7–9].

The biomechanical properties of an elasticity factor of 2.5 with a decrease in tensile strength of 70% after wetting makes fleece-bound sealants especially suitable for sealing of dynamically expanding systems like lung tissue [12]. Another advantageous feature of the product is its histocompatibility and the lack of toxicity of collagen carriers in combination with fibrin glues [12]. Animal studies have confirmed, that significantly fewer adhesions can be detected on serosal surfaces, covered with TC [22], whereas extensive tissue reactions and adhesions have been reported after the use of bovine pericardial strips [14,23,24].

From all these features, TC seems to be a valuable tool for prevention and treatment of air leaks after lung surgery. In order to obtain a scientifically based background on its actual value, this multi-centre, open, randomised and prospective trial was initiated. External monitoring of the study was performed to guarantee highest possible data accuracy.

Part of the protocol was prerandomisation treatment with conventional measures such as limited stapling and suturing in case of air leak degree 3. This was decided as an ethical precaution to provide maximal patient safety, although it also left an unexpected narrow therapeutic window to demonstrate any positive effects of the product.

No attempts were made to compare length of hospital stay, since this parameter is influenced by many other, sometimes not medically based factors.

The fact that five different institutions from four different countries participated in the study allowed one to ultimately have data which are representative of a general standard of contemporary lung surgery. An interesting finding was the high proportion of 52% of all patients achieving complete air tightness after standard surgery. This unexpectedly high percentage however influenced the final analysis in a way, that no significant difference for incidence of air leaks was found after 48 h between the standard and the treatment group when all patients were analysed. It was also demonstrated that a prophylactic use of an additional sealant after having achieved air tightness with standard surgery is not of any value, since the incidence of secondary air leaks at least in a standard population undergoing lobectomy is low.

On the contrary, analysis of the subgroup of patients presenting with proven air leak after lobectomy showed, that the use of TC resulted in a clear reduction of the degree of intra-operative air leak intensity, which was followed by a lower air leak intensity and a shorter duration of air leaks in the postoperative course. Although the semi-quantitative assessment of air leakage could be affected by some observational bias, all the differences were statistically significant.

Compared to other controlled studies published on the topic, this is a striking finding. Although Porte and Wain [8,9] have reported a significant reduction in both intra-operative and postoperative air leakage using a synthetic hydrogel sealant, they had to observe an increased rate of intra-thoracic infections appearing as localised empyemas, whereas the only intra-thoracic infection in this series, referred to as ‘empyema’ in Table 4, was presence of staphylococci in the drainage, which was successfully treated with antibiotic therapy only.

Wong and Goldstraw have tested fibrin glue in patients with established air leaks, but did not find any benefit regarding postoperative air leakage [6]. However, they have used length of chest tube drainage and length of hospital stay, both being very vague parameters for measuring the effects of their therapy.

As mentioned above, buttressing with pericardial strips can only be used in a prophylactic way, and has no place for treatment of already established air leaks. In a multi-centre randomised trial on different lung resections Miller and colleagues [17] found no statistical differences between buttressed and non-buttressed patients.

In summary, the findings of this trial demonstrate that postoperative air leakage after standard lobectomy can be found in almost every second patient and that the use of the fleece-bound sealant TC is a safe procedure. There is no evidence that a prophylactic use of TC in patients without established air leak is of value, but there is clear evidence that the therapeutic application of TC in patients with established air leak results in a reduced intensity and duration of these air leaks.

	References

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

 

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