Study about the ability of the pulmonary aerostasia, in animal model, using differents parenchymal pulmonary types of the sutures

Abstracts

INTRODUÇÃO: A busca de um modelo perfeito de aerostasia pulmonar, após cirurgias que envolvam ressecções parciais, permanece um desafio para a prática da cirurgia torácica. OBJETIVO: Avaliar e comparar, em um modelo animal (suínos), a eficácia de quatro diferentes tipos de sutura pulmonar em manter aerostasia. MÉTODO: Estudo experimental, ex vivo, em pulmões de suínos, realizado no biotério da Universidade de Caxias do Sul. Quatro tipos de sutura pulmonares foram avaliadas: tipo 1, sutura manual com fios cirúrgicos absorvíveis; tipo 2, grampeador exclusivo; tipo 3, grampeador recoberto por pericárdio bovino e tipo 4, grampeador recoberto por cola biológica. As suturas foram submetidas a níveis crescentes de pressão, que variaram de 10cmH2O a 60cmH2O. O teste do borracheiro avaliou o hermetismo das suturas. RESULTADOS: A média de pressão em que se observou perda do hermetismo pulmonar foi de 29cmH2O no tipo 1 (n = 10); 38,5cmH2O no tipo 2 (n = 10); 44cmH2O no tipo 3 (n = 10) e 51,4cmH2O no tipo 4 (n = 10). A comparação entre as médias mostrou diferença estatística apenas entre as suturas tipo 1 e as suturas tipo 3 e 4, p = 0,04 e p < 0,01. CONCLUSÃO: As suturas pulmonares com grampeadores revestidos por pericárdio bovino ou recobertos por cola biológica, quando comparadas às suturas que utilizaram fio cirúrgico isoladamente, mostraram maior eficácia em manter aerostasia pulmonar em pulmões de suínos. No entanto, não há diferença na eficácia em manter aerostasia pulmonar de suínos, quando se utilizaram suturas com grampeadores isolados ou revestidos por pericárdio bovino ou cola biológica.

Cirurgia torácica; Cola biológica; Grampeadores

ORIGINAL ARTICLE

Study about the ability of the pulmonary aerostasia, in animal model, using differents parenchymal pulmonary types of the sutures^*

Darcy Ribeiro Pinto Filho (te-sbct)

Professor of Thoracic surgery, Doctor of Pulmonology and Specialist as designated by the Brazilian Society of Thoracic Surgery

^{Correspondence}

ABSTRACT

BACKGROUND: The search for an ideal procedure to accomplish aerostasis, after partial surgical resection of the lung parenchyma, remains a practical challenge for the thoracic surgeon.

OBJECTIVE: The objective of this study was to compare the ability of four types of parenchymal pulmonary sutures in preventing air leaks, using a porcine model with incremental endobronchial pressures.

METHOD:Ex vivo experimental study in porcine lungs (n = 5) at the Laboratory of Experimental Surgery of the Universidade de Caxias do Sul. Four different parenchymal pulmonary types of suture were analyzed: type 1 (absorbable suture), type 2: (stapled suture), type 3 (stapled suture with bovine pericardium) and type 4 (stapled suture with biologic glue). The surgical sutures (n = 40) were exposed to different intrabronchial pressure levels, varying from 10 cmH₂O to 60 cmH₂O. The presence of air leaks along the suture line was verified through the water seal maneuver.

RESULTS: The mean intrabronchial pressure level needed to cause suture line air leaks for each type were: type 1 (n = 10): 29 cmH₂O; type 2 (n = 10): 38.5 cmH₂O; type 3 (n = 10): 44 cmH₂O; and type 4 (n = 10): 51.4 cmH₂O. The comparison between the mean intrabronchial pressure level of type 1 and of types 2 and 3 sutures was statistically significant, respectively: p = 0.04 and p = 0.01. However, the comparison between types 2, 3 and 4 did not show statistic significance (p > 0.05).

CONCLUSIONS: The pulmonary suture covered by biologic glue demonstrated more resistance to incremental levels of intrabronchial pressure. Parenchymal pulmonary sutures using stapled suture exclusively or stapled with bovine pericardium or biologic glue demonstrated an increased ability to avoid air leaks if compared to absorbable sutures in a model of porcine lung with incremental levels of intrabronchial pressure. There were no differences between stapler exclusively or stapler and bovine pericardium or biologic glue.

Key words: Experimental study. Thoracic surgery. Biologic glue. Staplers.

Acronyms and abbreviations used in this article

ANOVA – Analysis of variance

95% CI – 95% Confidence Interval

PTFE – Polytetrafluoroethylene

SPSS – Statistical Package for Social Sciences (program for statistical calculations)

Introduction

Air leakage through the bronchial stump or pulmonary parenchyma and the filling of pleural space by the remaining lung is one of the greatest intraoperative and post-surgical problems faced by surgeons performing partial pulmonary resection (lobectomy, segmentectomy, or wedge resection) or (more recently) lung reduction surgery. It is known that morbidity (from pleural infection and sepsis), time of hospitalization and mortality related to pulmonary surgery procedures increase considerably when post-surgical air leakage occurs.⁽¹⁾ Since the 1950s, the use of non-absorbable sutures, adequate blood irrigation of the bronchial stump and coverage of the sutured bronchus with pedicle flaps of intrathoracic tissue (parietal pleura, pericardial fat, intercostal muscles) has reduced the incidence of fistulas in the bronchial stump from 50% to the current range of 1.6% to 6.8%.^(2,3)

However, bronchopleural fistulas related to pulmonary parenchyma are sometimes very difficult to control. This difficulty is one of the factors that motivated us to develop this study.

The emergence of mechanical staplers and their use in pulmonary surgery was, undoubtedly, a significant landmark in the evolution of surgical technique for pulmonary resection.⁽⁴⁾ Some of the advantages of surgical stapling are more effective closure and reduced surgical time.⁽⁵⁾ In addition, stapling allows more exact delimitation of fissures in partial pulmonary resection, surgery for bullous emphysema and lung reduction surgery.⁽⁶⁾

The use of staples alone effectively increases lung integrity. However, some air leakage may still occur, especially at stapled corners, during intraoperative pulmonary re-expansion. This air leak is more significant in patients with pulmonary emphysema, due to the inherent loss of pulmonary elasticity.⁽⁷⁾ In light of these facts, the current recommendation is to cover the staple line with a substance that achieves a less permeable suture. The best results have been obtained with bovine pericardium and biological glue.^(8-11)

While we were attempting to solve this problem, new studies describing various techniques, such as the use of staples covered with bovine pericardium or fibrin glue and the inversion of the emphysematous walls of the bullae, were published.^(6-12)

Cooper et al. returned to the method proposed by Brantigan et al., namely that of reducing lung volume to allow better diaphragmatic performance in emphysematous patients, combining the challenge of operating on lungs that are extremely compromised by the emphysematous disease with that of maintaining a suture integrity in tissue that has practically no elastic support.^(6,13) In a population of emphysematous patients submitted to lung reduction, Cooper himself showed the importance of covering the staple line with bovine pericardium, which, according to his observation, could virtually eliminate post-surgical air leakage.⁽⁷⁾

A review of the literature revealed heterogeneous results regarding the ability of the various methods to increase pulmonary integrity and presented no comparative studies.

The search for a more efficient model in the prevention of post-surgical air leakage in surgery involving pulmonary parenchyma led us to test, in pigs, four types of pulmonary suture. The pigs were submitted to increasing intrabronchial pressure levels after which we determined air leakage through the suture line using a submersion test ("tire test").

The experimental model assessed and compared, ex vivo, porcine pulmonary integrity resulting from the use of various suture methods. We used and compared the following techniques: manual pulmonary closure with absorbable sutures, pulmonary suture exclusively with staples, pulmonary suture with staples in which the staple line was covered with bovine pericardium and pulmonary suture with staples in which the staple line was covered with biological glue.

Method

A total of 40 lung operations were performed on 5 pigs over a 5-week period. The 4 types of pulmonary suture were compared in terms of their ability to maintain an impermeable seal (lung integrity) when submitted to increasing intrabronchial pressure levels. Comparisons were made based on the results of a submersion test ("tire test").

Mean total time for resection of the lung block, suturing and pressure test was 45 minutes.

The study was performed at the Vivarium of Universidade de Caxias do Sul-RS. All 5 pigs were submitted, in rotation, to 4 different types of ex vivo pulmonary suture.

The animals were treated according to the Guide for care and use of laboratory animals (NIH number 80-23, 1978, revised on 1985).

Suture types

Suture type 1: Continuous hemostatic suture with separate "U" stitches, 5 mm apart, with absorbable sutures (chrome-plated catgut 0000), closing a 6-cm incision.

Suture type 2: Exclusive Linear Cutting Staples (Auto Suture International, Inc., Jomhédica, Porto Alegre, Brazil), closing a 6-cm incision.

Suture type 3: Linear Cutting Staples, covered with bovine pericardium harvested by the surgeon during the operation (Biopatch-biological graft of bovine pericardium; Biomedical Equipamentos e Produtos Médico-cirúrgicos Ltda., São Paulo, Brazil),closing a 6-cm incision.

Suture type 4: Linear Cutting Stapler, covered by 1 ml of sealing fibrin adhesive (Beriplast^® P-Centeon Farmacêutica-São Paulo-Brasil) sprayed on the suture line, closing a 6-cm incision.

Study design

Four types of pulmonary suture were used (on each side) at the previously identified sites (apical, superior medial, inferior medial and basal). This ensured equal distribution, as well as rotation of suture types, on both lungs.

After the completion of all suturing, unilateral pulmonary expansion was induced. Positive pressure was increased in 5-cm H₂O increments. Pressure levels were verified on the ventilator manometer. The proposed lower limit was 10-cm H₂O, and the upper limit was 60-cm H₂O. The contralateral mainstream bronchus was closed during the inflation process.

The immersion test is defined as submersion of the pulmonary suture in an isotonic saline solution and 10-second application of positive intrabronchial pressure, during which, air leakage through the suture line is monitored.

At the limit of each pre-established expansion, there was a 10-second end-inspiratory pause, during which air leakage through the sutures was monitored. The immersion test was considered positive when any air leakage was observed through the sutures. The lowest pressure level at which air leaked was recorded. The test was considered negative when no air leakage occurred at the pre-established maximum pressure limit (60-cm H₂O).

An airtight seal (pulmonary integrity) was defined as the absence of any air leakage through the suture line at any of the progressively increasing positive pressure levels applied during the immersion test.

Statistical analysis

In order to compare degrees of intrabronchial pressure that might produce air leakage among the four types of suture, the ANOVA test was used with a Gauss distribution and a statistically significant result was found with values of p < 0.05. Tukey test was used to differentiate among the groups. The sample size was calculated to reach an alpha-error of 0.05 and a beta-error of 0.2.

Data were processed with the SPSS v 8.0 program.

Results

Considering the four types of suture evaluated, the mean intrabronchial pressure at which pulmonary integrity was lost was 40.75-cm H₂O, with a standard deviation of 14.08 and 95% CI of 36.25-45.25. Means for loss of integrity among the different types of suture are shown in Table 1.

Tukey test revealed statistically significant differences in mean pressure at which loss of pulmonary integrity was observed only between suture types 1 and 3 and between suture types 1 and 4 (p=0.04 and p=0.01, respectively). No significant differences were found among suture types 2, 3 and 4, or between suture types 1 and 2 (Table 2).

The data in Table 1 points to a trend toward greater resistance when staple sutures were used and covered with bovine pericardium or biological glue (types 3 and 4; Figure 1).

Discussion

Analysis of the results from the experimental models confirms reduced resistance when closures were made manually using absorbable suture. Due to this limitation, this type of suture is rarely used in partial pulmonary resection, resection of bullous emphysema or lung reduction. In contrast, the use of staples has become widespread in such surgeries and has been integrated into the routine of most thoracic surgery departments worldwide.^(2,4,14)

In a study of 80 patients submitted to pulmonary resection (excluding lung reduction), Miller et al. compared the efficacy of uncovered staple sutures to that of staples covered with bovine pericardium.⁽¹⁷⁾ The authors found no statistically significant difference between the 2 groups in length of time air leakage was observed in the post-surgical period or length of time that pleural drains were required (p > 0.05).

Venuta et al. and Vaughn et al., assessing the use of bovine pericardium and polytetrafluoroethylene (PTFE) combined as a reinforcement of the pulmonary suture, confirmed that this method was more efficacious in preventing post-surgical air leakage than was the use of electrocauterization and absorbable sutures (p < 0.01).^(18,19)

Jatene et al. used mechanical sutures (staples) in 150 patients submitted to bronchial suture, both pulmonary parenchymal and vascular, totaling 186 procedures.⁽²⁰⁾ These patients, who had malignancies, suppurative diseases and congenital malformations, presented no bronchial fistulae after mechanical suture.

The theoretical supposition that coverage of the staple line with the available material might increase effectiveness of pulmonary integrity seems reasonable. Our experimental model presented no statistically significant differences in degree of resistance under increased intrabronchial pressure between uncovered staple sutures and those covered with bovine pericardium or biological glue (p > 0.05).

Topical application of fibrin glue, or biological glue, to reduce post-surgical air leakage, has been used in lung surgery since the 1970s, especially in Europe. Thetter, along with Turk et al., were among the first to report more effective control of air leakage with pulmonary sutures in which biological glue was used.^(21,22) Thetter described the use of the glue in thoracotomy, both alone and combined with abrasive pleurodesis, as a way of encouraging further pleurodesis in patients with spontaneous pneumothorax. He compared this group of patients with controls found in the literature (on whom no glue had been used) and concluded that mean length of time for the permanence of drains was lower in the treated group. The same author observed no statistically significant differences in length of time that pleural drains were required between patients who had been submitted to pulmonary resection (and whose parenchyma had been covered with fibrin glue) and those (controls in the literature) on whom such sealers had not been used. The study conducted by Turk et al., after submitting two groups of rats to a traumatic section of pulmonary parenchyma, observed that covering the lesion with fibrin glue provided more resistance to pressure in the airways.⁽²²⁾ The use of the same model in patients submitted to pulmonary resection, and intraoperatively tested in terms of suture tolerance to positive pressure showed that in patients whose suture line had been covered with biological glue the suture resistance was 36% higher than in the group in which no reinforcement with biological glue was used (p < 0.05).

Nomori and Horio showed the possibility of extrapolating results of experimental surgery to human surgery.⁽²³⁾ Their model used pig lungs and staple sutures covered with formaldehyde and glutaraldehyde and submitted to increasing pressure levels. At the upper limit of 60-cm H₂O, no air leakage was observed through the suture line. The use of the same model in ten patients with emphysema confirmed the pulmonary integrity obtained with a staple suture covered with formaldehyde and glutaraldehyde.

In a classical article, Mouritzen et al. assessed 114 patients submitted to lung resection (classified as either lobectomy or pneumonectomy).⁽²⁴⁾ In the group of patients submitted to lobectomy (n = 63) the parenchymal suture was reinforced with biological glue (Beriplast^®) and suture resistance, as defined by the maintenance of pulmonary integrity, was shown to be 67.7%. In the control group, 48.4% achieved pulmonary integrity (p<0.01; 95% CI = 58%-98%). Another variable assessed in this study was the proportion of air leakage in the post-surgical period. In the group of patients submitted to lobectomy and application of biological glue, the incidence of air leakage was 38.7% compared with 65.6% in the control group (p<0.05). However, no statistical difference in the length of time the air leakage was present was seen between the two groups: 4 days in the biological glue group and 5 days in the control group.

A clinical application for these sealers was shown in a more recent study, conducted by Wong et al., who assessed the effects of fibrin glue in reducing alveolar air leakage after thoracotomy.⁽²⁵⁾ A total of 66 lobectomy, segmentectomy or pulmonary decortication patients who presented moderate to persistent intraoperative air leakage, despite the use of conventional control actions for this situation, were split into two 33-patient groups and suture reinforcement with biological glue was used in the study group. The mean length of time that pleural drains were required and the mean length of hospitalization was 6 and 8 days, respectively, in the biological glue group and 6 and 9 days, respectively, in the control group. The authors concluded that there was no advantage in using biological glue in addition to conventional methods for air leakage control and noted the high cost of the fibrin sealers.

The possibility of using other sealer options has been shown in a number of literature reports.^(26-29) In a model similar to ours, Kjaergard et al. submitted a group of pigs to pulmonary suture with the application of autologous fibrin (Vivostat-ConvaTec, Skillman, NJ, USA), and used a control group in which the pulmonary sutures were covered with a 20% solution of human albumin.⁽³⁰⁾ Under increasing positive airway pressure, the resistance of each material was tested using the immersion test and the autologous fibrin was found to be the most effective in preventing air leakage (p<0.01). The possible use of autologous material represents a promising future for the sealers. Hepatitis B, hypotension, anaphylactic reaction, hemorrhage and infection, all potential side effects of using biological fibrin glue, might be avoided by the use of fibrin manufactured from blood drawn from the patient involved.

The use of fibrin glue in pulmonary tissue is an issue to be discussed. The peculiar characteristics of the lungs, organs filled with air spaces and a large volume of blood and which change their volume with every breath, makes the application and adherence of a material to its surface a challenge. During the sealer polymerization, two types of chemical bonds are formed inside the adhesive: an internal bond of the sealer to itself, and an external bond of the sealer to the tissue. The internal bond is the stronger. If any movement occurs at the surface, the substance may change its configuration, and will no longer adhere. This must be kept in mind when applying biological glue to the lung surface. The application site should as dry as possible, and the lung should be stabilized by bronchial tweezing until the chemical reaction is complete.⁽³¹⁾

One feature that limits the extrapolation of the results of the model assessed in our study is the use of healthy lungs, with no pulmonary emphysema and, therefore, with normal elasticity. However, one might ask if we could do without reinforcement along the staple suture line in patients with normal lungs submitted to resection. Even though it was not the objective of this study, it seems only fair to reflect upon this, especially if we consider the cost of such materials. The 6.0 linear cutting stapler with one loading costs approximately R$1,500 and the biological glue costs approximately R$300 per ml.

In future studies, it may be necessary to create an experimental animal model of pulmonary emphysema in order to test this suture method in diseased lungs. Such studies are warranted if we are to mirror or represent the features of the patient population most commonly submitted to pulmonary surgery.

Pulmonary staple sutures covered with bovine pericardium or biological glue presented greater efficacy in maintaining the pulmonary integrity of pig lungs than did traditional sutures. However, no difference was found in terms of efficacy in maintaining the pulmonary integrity of pig lungs between uncovered and covered (with bovine pericardium or biological glue) staple sutures.

References

Submitted: 27/05/2003. Accepted, after revision: 31/07/2003.

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*

Research performed at Universidade de Caxias do Sul, RS.

Publication Dates

• Publication in this collection
  02 Mar 2004
• Date of issue
  Oct 2003

History

• Received
  27 May 2003
• Accepted
  31 July 2003