Asian Cardiovasc Thorac Ann 2004;12:61-64
© 2004 Asia Publishing EXchange Ltd
Limiting Pericardial Adhesions after Coronary Artery Bypass: Experimental Study
Kamalas Saha, FRCS,
Winston McEwan, MBChB,
Frank A Frizelle, FRACS1,
Harsh Singh, FRCSI
Department of Cardiothoracic Surgery
1 Department of General Surgery, Christchurch Hospital, Christchurch, New Zealand
For reprint information contact: Frank A Frizelle, FRACS Tel: 64 3 364 0640 Fax: 64 3 364 0352 Email: frank.frizelle{at}chmeds.ac.nz Department of Surgery, Christchurch Hospital, Riccarton Ave, Christchurch, New Zealand.
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ABSTRACT
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Retrosternal pericardial adhesion formation constitutes a major hazard during re-do coronary artery surgery. To determine whether an onlay parietal pleural flap over the internal thoracic artery bed would reduce pericardial adhesions after coronary artery grafting, 16 sheep underwent a median sternotomy and both internal thoracic arteries were harvested. On the randomly selected study side, a dissected pleural flap was used to cover the internal thoracic artery bed, the opposite side was left uncovered as a control. Half of the sheep were sacrificed at a median of 102 days (range, 93109 days), the remainder at a median of 176 days (range, 165183 days). Two independent observers blinded to the initial operation scored the degree of postoperative adhesions. There was a significant decrease in adhesion formation on the study side covered by the mobilized pleural flap, compared to the control side. There were no increases in pulmonary morbidity or sternotomy wound problems from raising the lateral pleural flap. This simple technique appears to be an effective method of preventing adhesion formation following coronary artery bypass grafting utilizing the internal thoracic artery.
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INTRODUCTION
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Re-do coronary artery surgery constitutes 10%20% of most current cardiac operations.1 Retrosternal adhesions resulting from previous surgery continue to be a challenge during sternal re-entry. The presence of these adhesions not only adds to the operating time but also increases the risk of damage to the heart, great vessels, and previously placed grafts.2 The reported incidence of damage to underlying structures at resternotomy is 2%6%, and such damage can be life threatening.3 Various techniques to prevent pericardial adhesions at the primary coronary artery bypass grafting (CABG) operation have been tried. Primary pericardial closure confers some protection to the heart and underlying structures, but it is rarely practiced because of the danger of exerting external pressure on the graft.4,5 Biological or synthetic pericardial substitutes, pharmacological agents, and an internal thoracic artery (ITA) wrap have not been widely adopted due to their various limitations.610
The pathophysiology of adhesion formation is not fully understood. Mesothelial cells possess fibrinolytic activity that has a potential role in preventing adhesion formation.10 Areas denuded of these cells, such as the site of ITA harvest, can form dense adhesions. A new operative procedure is proposed, involving dissection of the parietal pleura (of mesothelial origin) laterally from over the ITA before harvesting, and using this flap of pleura to cover the ITA bed at the end of CABG. This animal study was designed to observe adhesion formation over the chest wall with and without covering of the ITA bed with a pleural reflection.
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MATERIALS AND METHODS
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Prior approval was obtained from the Canterbury University Animal Ethics Committee. All animals received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and the "Guide for the Care and the Use of Laboratory Animals" prepared by the National Academy of Science and published by the National Institutes of Health (NIH publication no. 8523, revised 1996). All procedures were performed according to the Heath Research Council of New Zealand Guidelines on Animal Experimentation.
Using standard techniques, 16 sheep underwent general anesthesia, sternotomy, and harvesting of the ITA pedicle. After overnight fasting, the sheep were anesthetized with intravenous thiopentone and placed on the operating table with endotracheal intubation. General anesthesia was maintained during controlled mechanical ventilation with an inspired gas mixture of oxygen and nitrous oxide, supplemented with halothane as required. Perioperatively, antimicrobial prophylaxis was used (penicillin and streptomycin). The sheep were placed in the supine position and a sternotomy was performed using an aseptic surgical technique. The right and left ITA were harvested as pedicled grafts. Prior to dissecting the ITA, a parietal pleural flap was dissected on one randomly allocated side (study side), reflected over the ITA laterally, and carefully preserved (Figure 1
). On the other side, a standard pedicled ITA was dissected. The distal end of the ITA was clipped with a hemoclip and divided. The pericardium was opened and both ITA were fixed to the surface of the heart using 4/0 polypropylene suture to simulate CABG. The pericardium was kept open. The dissected pleural flap on the study side was used to cover the raw ITA bed and sutured back to the periosteum of the sternal edge using 4/0 Monocryl suture (Ethicon, Johnson & Johnson, Somerville, NJ, USA). The control side was left uncovered. The sternum was closed using steel wires after placing a single 22F mediastinal drain. The drain was removed the following morning. The same surgeon operated on every sheep.
Postoperatively, the animals were cared for at the Canterbury Medical School Animal Laboratory facilities for two weeks, and transferred to a farm when satisfactorily recovered. Half of the sheep were sacrificed after approximately 3 months (range, 93107 days; median, 102 days), and the others were sacrificed after approximately 6 months (range, 165183 days; median, 176 days). The sheep were killed humanely using intravenous pentobarbitone, the chest was reopened, and two independent observers scored the adhesions on each side. The adhesions were scored as: grade 0, no adhesions between the chest wall and underlying heart; grade 1, flimsy adhesions separated easily by a sweep of the finger, no instrument required (Figure 2
); grade 2, requiring dissection with scissors but easily dissected by combined finger dissection and sharp dissection; or grade 3, dense adhesions only separated by sharp dissection using a knife and scissors (Figure 3
).12 To prevent bias in adhesion scoring, 2 or 4 sheep were operated on each day and either side was used as the study side alternately (Table 1
). Adhesion scoring was performed on separate days by the two operators, one of whom was blinded to the initial procedure, the other had performed the surgery. Neither had access to the previous operative records at the time of resternotomy. When all animals had been scored for adhesions, they were matched to their operative records. The data were analyzed using the Sign Test on differences in scores within each animal.
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RESULTS
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One sheep died immediately postoperatively and was not included in the study. Postmortem examination was negative for any cause. Another animal was operated on a week later to complete the study. One sheep (No. 2) died at the farm on day 95, 14 days earlier than the scheduled study date. The animal was examined on the day of death and included in the study (Table 1
). The adhesion scores recorded by the two independent observers were the same in all except 2 animals. The first observer scored 1 and the second scored 2 for the study side in No. 11, whereas the first observer scored 2 and the second scored 1 for the study side in No. 12. In both animals, the higher adhesion score of 2 was used for analysis (Table 2
). In the group sacrificed at 3 months, most of the study sides had adhesion scores of 01, while the control sides usually scored 3. In the animals checked at 6 months, two had a score of 2 on the study side with a score of 3 on the control side, all others scored 01 on the study side and 3 on the control side. Statistical analysis of the data showed there was a significant decrease in adhesion formation on the study side compared to the control side ( p = 0.0078).
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DISCUSSION
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Covering the ITA bed with a lateral flap of parietal pleura decreased the formation of adhesions between the raw surfaces of the dissected ITA and the underlying structures. There was still the problem of the right ventricle adhering to the sternotomy incision and intrapericardial adhesions, however, lateral dissection during which a patent ITA graft might be damaged was improved by the reduction in adhesions. This technique addresses the limitations of previous methods to decrease pericardial adhesions as, unlike pericardial closure, there is no restrictive effect on the heart, thereby eliminating the possibility of tamponade and graft restriction.
Adhesions form as a result of the combination of the inflammatory response to injury, fibrin deposition over the exposed serosa, and absence of a mesothelial matrix, leading to fibrosis and adhesion between the parietal and visceral surfaces.13 When dissecting the ITA from the chest wall during CABG surgery, the pleura overlying the vessel is usually pealed away leaving a strip of chest wall devoid of pleura. The raw surface is a potential site for adhesions with underlying structures to form. In redo surgery, the problem of adhesions from the primary cardiac operation has prompted extensive research into ways of decreasing retrosternal adhesions. These include primary pericardial closure, use of pericardial substitutes, or pharmacological agents.4,14,15 Pericardial closure limits retrosternal adhesions following CABG but it can lead to hemodynamic instability, early cardiac tamponade from postoperative bleeding, extrinsic pressure on the grafts, and it may be dangerous in patients with impaired left ventricular function.4 Variable host responses to pericardial substitutes have been noted, including excessive fibrosis and calcification with difficulty in identifying coronary anatomy at reoperation.7,17,18 Some reports have indicated patch-related complications in approximately 1%.19 There are also concerns regarding the eradication of infection in the presence of a foreign body.3 Pharmacological agents also produce a variable response and there is a likelihood of washout during drainage of blood in the immediate postoperative period.
Individual response to injury can be extremely variable, affecting the extent of adhesion formation. This was observed in our model as in other animal studies.20 This limitation was avoided in our study by using a contralateral control in each animal, thereby accounting for individual variations in the degree of adhesion formation.
Mesothelial cells are known to have fibrinolytic activity, and areas denuded of these cells tend to develop fibrous adhesions that complicate reoperation.11 The raw surface due to ITA harvest is a potential site for dense adhesion formation. This was confirmed by the presence of dense adhesions on the control side in both groups in this study. The finding of minimal or no adhesions on the study side in most animals indicates that the pleural flap was effective in preventing adhesion formation. The same concept is applied effectively in thoracic surgery for the treatment of spontaneous pneumothorax (surgical pleurectomy). Covering the raw surface of the ITA bed may also decrease blood loss from this site. It is possible that harvesting the ITA in the extrapleural plane may achieve the same effect as dissecting a lateral pleural flap, because both techniques prevent a raw chest wall surface being exposed to the heart.
It was concluded that the parietal pleural flap is an effective method of limiting adhesion formation following primary CABG using the ITA. This technique is simple, safe, easily reproduced, and avoids the risk of infection from foreign materials. Moreover, this experimental model of bilateral ITA harvest to use one side as a control for the other side, can be used to test future techniques or agents for prevention of adhesions. Further developments are needed as this procedure only reduces the problems associated with lateral dissection.
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