Ann Thorac Surg 1999;68:913-918
© 1999 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Reduction of retrosternal and pericardial adhesions with rapidly resorbable polymer films
Naoki Okuyama, MDa,
Catherine Y. Wang, MDb,
Eric A. Rose, MDb,
Kathleen E. Rodgers, PhDa,
Eli Pines, PhDa,
Gere S. diZerega, MDa,
Mehmet C. Oz, MDb
a Livingston Reproductive Biology Laboratory, Department of Obstetrics and Gynecology, University of Southern California, Los Angeles, California, USA
b Division of Cardiovascular Surgery, Columbia University, New York, New York, USA
Address reprint requests to Dr Oz, Columbia-Presbyterian Medical Center, Milstein 7-435, 177 Fort Washington Ave, New York, NY 10032;
e-mail: mco2{at}columbia.edu
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Abstract
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Background. The formation of postoperative cardiac adhesions makes a repeat sternotomy time consuming and dangerous. Many attempts have been made to solve this problem by using either drugs to inhibit fibrinolytic activity or different types of pericardial substitutes. The results have not been satisfactory.
Methods. The efficacy of bioresorbable film prototypes made of polyethylene glycol (EO) and polylactic acid (LA) (EO/LA = 1.5, 2.5, and 3.0) in the prevention of adhesions after cardiac operations in canine models was tested. After desiccation and abrasion of the epicardium, a transparent bioresorbable film was placed over the heart. The pericardium was closed to allow intrapericardial adhesions (n = 32) or left open and attached to the chest wall to induce retrosternal adhesions (n = 17). Postoperative recovery was similar among the groups. Retrosternal and pericardial adhesions were evaluated at necropsy 3 weeks later by assessing area, tenacity, and density of the adhesions.
Results. In the control dogs, tenacious, dense adhesions were observed. In contrast, adhesion formation was reduced at all sites covered by the films. The bioresorbable films were efficacious in the reduction of adhesion formation between epicardium and pericardium or between epicardium and sternum after cardiac operation. The EO/LA 1.5 film most effectively prevented the early adhesions.
Conclusions. The bioresorbable films (EO/LA = 1.5, 2.5, and 3.0) significantly reduced adhesion formation, with EO/LA = 1.5 (Repel CV) being optimal. As the barrier was rapidly resorbed, the capsule formation induced by permanent barriers was avoided.
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Introduction
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At the time of reoperation in cardiac procedures, the risks caused by retrosternal adhesions include injury to the right ventricle, aorta, right atrium, innominate vein, and any aortocoronary bypass graft. These injuries often result in severe hemorrhage with significant morbidity and mortality [1–8]. Duncan and associates [9] reported that resternotomy is associated with a 2% to 6% incidence of major vascular injury. Dobell and Jain [10] reported that 88% of hemorrhages occurred after reoperative procedures following previous operations in which the pericardium was left open. The associated mortality was 39%, and the mortality after injury to the aortocoronary bypass graft was 56%. In addition, adhesions between the pericardium and the epicardium after pericardial closure will obscure epicardial architecture and landmarks, making prevention of these adhesions important.
Closing the pericardium after cardiac operation appears to show a reduction in adhesion formation. However, after cardiac procedures, pericardial closure is often not possible due to cardiac edema and the possibility of restricting right ventricular filling. Indeed, cardiac tamponade occurs more often after pericardial closure [5]. Many investigators have described materials that reduce adhesion formation in the retrosternal space [9, 11–20]. However, these materials are not commonly used clinically because of the capsule formation associated with their use or difficulties in their intraoperative application. In this study, the efficacy of the films, which are comprised of polyethylene glycol (EO) and polylactic acid (LA) and are rapidly bioresorbed, were evaluated for the reduction of adhesion.
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Material and methods
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Preparation of the films
Films of various EO/LA ratios (EO/LA = 1.5, 2.5, and 3.0), which were sterilized by ethylene oxide (gas) sterilization, were supplied by Life Medical Sciences, Inc (Edison, NJ). The film of EO/LA = 1.5, REPEL-CV, has been approved by the Food and Drug Association for cardiovascular surgical trail and the film of EO/LA = 3.0, REPEL, is under clinical evaluation in gynecologic operations. The bioresorbable barrier films evaluated in this study are block copolymers comprising LA and EO segments. These components have been used extensively in implantable, absorbable medical devices such as sutures and mesh materials. Because of its specific composition and molecular architecture, the film possesses defined mechanical strength, flexibility, rate of resorption, and biocompatabilty. As the EO/LA ratio of the film decreases, the resorption rate of the film is prolonged. Furthermore, the strength of the film increases as the EO/LA ratio is decreased. Thus, by varying the EO/LA ratio of the film, one can control the duration in which the film provides a temporary barrier to mechanically separate potentially opposing surfaces during the early phase of the healing process; adhesion formation is subsequently prevented. The films were desiccated at room temperature until the day of operation. Before use, the films were placed in sterile saline for 10 to 15 minutes to allow hydration.
Animal preparation
Forty-nine mongrel canines, 20 to 25 kg, were fasted 24 hours before operation. The dogs were quarrantined at least 14 days in the vivaria before operation. The following protocols were approved by the Institutional Animal Care and Use Committee of the University of Southern California and Columbia University. After endotracheal intubation, isoflurane (0.5% to 2%) was administered as a general anesthetic. During the procedure, the dogs were connected to pulse oximeters, blood pressure, and electrocardiogram equipment. A median sternotomy was performed using a sternal saw taking care to avoid injury to the underlying pleura and pericardium. Bleeding was controlled with electric cautery. The anterior pericardium was opened for 10 to 12 cm using sharp dissection.
Adhesion creation protocols
Two separate adhesion-inducing protocols were chosen to examine adhesions from the heart to the epicardium or posterior sternum, respectively.
In protocol 1, each section of the epicardium (central strip, apex, anterior left and right) was abraded 100 times with gauze until punctate bleeding developed. In control animals, four polypropylene sutures were placed in the pericardium bilaterally adjacent to each phrenic nerve. In treated dogs, the film was placed between the pericardium and the epicardium, and fixed to the pericardium adjacent to the phrenic nerves by four polypropylene sutures. The pericardium was closed using three interrupted sutures of 3-0 polyester-coated Dacron. The sternum was closed with wire. Air and blood were removed from the pleura using a suction tube while lungs were expanded by manual ventilation (pressure, 10 mm Hg). The suction tube was then immediately withdrawn. The fascia of muscle, subcutaneous tissue, and skin were closed.
In protocol 2, the anterior surface of the heart (anterior left, anterior right, central strip, and apex) and both sides of the retrosternal fascia were desiccated and abraded for 2 minutes with fine "0" sand paper. The desiccation/abrasion procedure was repeated once on each side with an interval of 5 minutes between procedures. After desiccation/abrasion procedure, six 2-0 polyester-coated Dacron sutures were placed on the pericardium 2 to 3 cm away from the cutting edge (two on each side, one on the top and one on the bottom). The pericardial edges were then bilaterally sutured into the corresponding sides of the chest wall and the sutures on the top and bottom were sutured into the sternum and xyphoid, respectively. The heart was then brought toward the sternum ensuring that the anterior surface of the right ventricle was in slight contact with the sternum. The pericardium was left open more than 5 cm (Fig 1 ) Next, the apex was lifted anteriorly to allow a 2- to 3-cm incision to be made on the posterior pericardium to avoid tamponade.
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Fig 1. Six 2-0 polyester-coated Dacron sutures were placed on the pericardium 2 to 3 cm away from the cutting edge; two on each side, one on the top through the sternum and on the bottom through xyphoid. The pericardial edges were then bilaterally sutured into the corresponding sides of the chest wall, and the sutures on the top and bottom were tied into the sternum and the xyphoid, respectively. The heart was then brought toward the sternum ensuring that the anterior surface of the right ventricle was in slight contact with the sternum. The pericardium was left open more than 5 cm.
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The surgeon was kept blinded as to which animal received barrier treatment or control until the last possible moment. In the control animals (n = 4), the sternum, muscles, and skin were closed. In the treated groups (n = 13), four sutures were used to attach the film to the four corners of the pericardium. The film was positioned from the anterior right to anterior left side before chest closure, again ensuring contact between the right ventricle wall and the posterior sternum.
Two 24F to 26F gauge chest tubes were placed on each side of the chest and were maintained approximately 48 hours after operation to evacuate residual blood and air.
Postoperative care
During the postoperative interval, the dogs were closely observed for signs of pain, lethargy, alterations, appetite, urination, defecation, and attitude. All dogs received 3 days of postoperative antibiotics. Pain medications were administered as indicated. The dogs were observed daily until necropsy 3 weeks after operation. After euthanasia by pentobarbital (Western Medical Supply Inc, Arcadia, CA) overdosage (120 mg/kg), adhesion formation between the pericardium and the epicardium or sternum was assessed by visual inspection, and measured and characterized using standard tenacity and density scores.
Evaluation of adhesion formation
Evaluation of adhesion formation between the pericardium and the epicardium were performed by the same two observers blinded to the treatment using a bilateral thoracotomy approach. Evaluations were performed at the following sections of the epicardium: central strip (base, mid, apex), anterior left, and right.
The area of adhesion formation, tenacity score, and density score were estimated at each site. Evaluation of adhesion formation between the sternum and the epicardium was performed using only the central strip region. The following grading system was used to evaluate the tenacity and density of the adhesions: tenacity (0 = no adhesions; 1+ = mild adhesions [easy to dissect manually]; 2+ = moderate adhesions [cohesive and can be dissected manually]; 3+ = severe adhesions [cohesive, requires sharp dissection] or nondissectable) and density (0 = no adhesions; 1+ = sparse adhesions; 2+ = moderate adhesions; 3+ = dense adhesions).
Statistical methods
The Student’s t test and Mann Whitney were used to analyze the area of adhesion formation. A p value of less than 0.05 was considered significant. The Mann Whitney test was used to analyze the tenacity score and density score of adhesion. A p value less than 0.05 was considered significant.
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Results
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The chest operation was conducted on 49 dogs, of which 32 underwent protocol 1 with pericardial closure and 17 were operated on according to protocol 2 with retrosternal suspension. All dogs survived operation until necropsy.
The bioresorbable films significantly reduced adhesion area, density, and tenacity as are seen in both models (Table 1). In model 1, moderate to severe tenacious adhesions were observed between the epicardium and the pericardium in the control canines. Typically, dissection of the pericardium from the epicardium was very difficult. In contrast, the areas of adhesion formation in the treated groups were significantly smaller than in the control group (Fig 2). The mean tenacity score and the mean density score of adhesions formed in the treated groups were significantly less than for the control group (Fig 3). There were no complications (eg, bleeding, mediastinitis, or pericarditis) observed in the 32 evaluated dogs.
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Table 1. Evaluation With the Area, Density, and Tenacity of Pericardial Adhesions in Canine Model-1 and Retrosternal Adhesions in Canine Model 2
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Fig 2. Mean adhesion (Adh) area for each group in model 1, pericardial adhesions, shown as mean ± standard error of the mean. Each treatment group was compared with the control group (*p < 0.05) and analyzed by Mann-Whitney test. (EO = polyethylene glycol; LA = polylactic acid.)
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Fig 3. Overall mean adhesion scores for tenacity and density for each group in model 1, pericardial adhesions, shown as mean ± standard error of the mean. Each group was compared with the control group (*p < 0.05) and the statistical analysis was done with Kruskal-Wallis and Mann-Whitney tests. (EO = polyethylene glycol; LA = polylactic acid.)
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In model 2, the areas of adhesion formation between the sternum and the central strip of the epicardium in the treated groups were also significantly reduced compared with the control group (Fig 4). The mean tenacity score and the mean density score of adhesions formed in the treated groups were significantly less than for the control group (Fig 5). Specifically, the EO/LA 1.5-treated animals were completely free of adhesions, with a glistening cardiac surface. Although no film remnants were observed in any animal at necropsy, some early segments were noted from the chest tube drainage within the first 2 days in the EO/LA 2.5 and 3.0 animals. No remnants were seen in the chest tube drainage from the EO/LA 1.5 animals, presumably due to less rapid biodegradation, suggesting that this material may be superior (less risk for clogging of chest tube drainage).
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Fig 4. Mean adhesion (Adh) area for each group in model 2, retrosternal adhesions, shown as mean ± standard error of the mean. Each treatment group was compared with the control group (*p < 0.05) and analyzed by Student’s t test. (EO = polyethylene glycol; LA = polylactic acid.)
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Fig 5. Overall mean adhesion scores for tenacity and density for each group in model 2, pericardial adhesions, shown as mean ± standard error of the mean. Each group was compared with the control group (*p < 0.05) and the statistical analysis was done with Kruskal-Wallis and Mann-Whitney tests. (EO = polyethylene glycol; LA = polylactic acid.)
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Comment
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In these studies, the efficacy of bioresorbable barriers in reducing adhesion formation between the epicardium and the pericardium or sternum was assessed in canine models. In addition to seeking an antidote to the scar formation that complicates reoperation in cardiac procedures [1–9], we were interested in studying the time course of adhesion formation. We hypothesized that if only the very early stage of postoperative adhesions were prevented, we would still observe a dramatic reduction in later scar formation as the scaffold (eg, fibrinous adhesions) on which the scar is created would never have been laid. This study has shown the dramatic changes between the controls and the animals treated with films, especially with the EO/LA 1.5 film-treated animal (Fig 6). This paradigm for understanding the time course and method for scar formation has been well studied in the gynecologic field where adhesion formation has a dramatic impact on clinical symptoms and surgical practice [21]. Previous studies have evaluated the ability of a variety of agents to reduce or prevent adhesion formation after cardiac operation. Sheep [14, 18, 22, 23] and rabbit models [19] have also been used, but the canine model is used in the majority of the studies [9, 11–17, 20]. Studies conducted using a canine model described adhesions between the epicardium and the pericardium. In contrast, adhesions in humans typically form between the sternum and the pericardium and epicardium. Unlike human chest anatomy, where the heart is fixed in place by the surrounding pleura, creation of retrosternal adhesions in a canine model was difficult due to the space between the sternum and the heart and it required that the epicardium be brought into proximity with the sternum by suturing the pericardium to the sternum. This technique also kept the lungs separated from each other anteriorly, making it a more analogous situation to human chest anatomy.
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Fig 6. Necropsy taken 24 days after operation from control animal and bioresorbable film. Severe and nondissectable adhesion was seen in the control animal (A). A heart free of adhesions can be seen in the polyethylene glycol/polylactic acid 1.5-treated animal (B).
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Previous studies have reported the results of attempts to prevent adhesions using nonresorbable materials, such as polytetrafluoroethylene (PTFE) membrane [11–14], bovine pericardium, or equine pericardium [15–18]. These pericardial substitutes were evaluated by assessing adhesion formation between the epicardium and the substitute. Although adhesions are reduced, the resulting capsule formation obscures anatomic landmarks and creates a second level of adhesions that can be technically challenging to dissect. Various fibrinolytic drugs [19] have been used in rabbit epicardial abrasion and retrosternal adhesion models. The pericardium is left open and the pericardial space is filled with fluid. The studies have demonstrated efficacy; however, maintaining the solutions in the correct anatomic position will be difficult in humans, especially if a pleural space is opened or chest tubes are used. The bioresorbable films tested in this report were evaluated for adhesion prevention using a rabbit model similar to that described above and revealed significant reductions in adhesion formation between the sternum and the epicardium [24]. A resorbable polyhydroxy-butyrate material has been studied in 23 sheep necropsied between 2 to 30 months after operation [21]. Moderate adhesions were formed between the sternum and the pericardium in all 5 control sheep (100%). In the 18 treated sheep 14 had no adhesions, 3 (16.7%) had loose adhesions, and 1 (5.6%) had moderate adhesions. This patch reduced the formation of retrosternal adhesions and was completely absorbed at the time of necropsy. Light microscopy and electron microscopy were used to evaluate the quality of adhesions formed. A layer of mesothelium-like cells was already present in the early specimens. Polyhydroxybutyrate appeared to be slowly phagocytosed by macrophage. Lymphocytes and platelet were rare. In the current investigation, we compared hematoxylin- and eosin-stained specimens of the right ventricular wall from beneath the sternum between treated and untreated dogs 72 hours after operation. The histologic examination demonstrated a markedly reduced inflammatory response in the treated animals (Fig 7). This reduced inflammatory response may result in less adhesion formation [25].
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Fig 7. Hematoxylin and eosin-stained specimens of the right ventricular wall from beneath the sternum 72 hours after operation. The reduced inflammatory area and amount of inflammatory cells were seen in the polyethylene glycol/polylactic acid (EO/LA) 3.0 film-treated animal (right) compared to the control animal (left). (original magnification, x120.)
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Clinically, many approaches have been used to reduce adhesion formation within the retrosternal space. These materials could be classified into four groups: prosthetic membranes, xenograft membranes, solutions containing pharmacologic agents, and resorbable membranes. Prosthetic membranes include silicone rubber, PTFE membrane, polyethylene film, and Dacron mesh [11–14]. Although the efficacy of PTFE membrane is recognized, clinical use has been limited by concerns over the permanence of this sheet and the resulting formation of a fibrous capsule. This poses a potential problem for pediatric patients as the heart grows and leaves a foreign body in place, which could predispose to infection over time. Furthermore, PTFE is not transparent and may interfere with visualization of the cardiac architecture during operation. Also, many investigators have reported the efficacy of xenograft membranes, including equine pericardium and bovine pericardium [15–18]. However, these membranes are also permanent and opaque. The current study has displayed the benefits of film transparency, which provides a clear vision of the field before closing the sternum (Fig 8). The efficacy of several solutions including hydrophilic polymer solution [11], hyaluronic acid coating solution [20], and solutions containing fibrinolytic drugs have been tested. Tissue plasminogen activator and its analog and streptokinase have been effective in reducing adhesion formation [19]. However, postoperative bruising, bleeding, and swelling were associated with administrations of streptokinase and the tissue plasminogen activator analog. The use of bioresorbable films may be limited in the event that if the weaker material fragments prematurely, it could be dislodged by fluid draining through the chest tubes. To avoid this, even sturdier films could be created, but the more permanent material may induce a reaction to itself in the pericardial space, an occurrence noticeably absent in these studies. The optimal duration for which early adhesions must be prevented to reduce longer term scar formation is unknown; however, evidence from general and gynecologic fields would indicate that even 6 to 12 hours may be sufficient [24]. Recognition of this time course makes use of bioresorbable films, which are free of capsule formation and do not appear to constitute a long-term infection risk, more appealing. Indeed, the increased efficacy noted in the lower EO/LA ratio may have been attributable to the material remaining in place longer. In summary, the bioresorbable films (EO/LA = 1.5, 2.5, and 3.0) were found to significantly reduce adhesion formation, with EO/LA 1.5 (Repel CV) being optimal. From a technical perspective, the films are transparent and, therefore, do not impede visibility during operation; however, we found that the film with an EO/LA ratio of 3.0 was too fragile for clinical use. The film of EO/LA = 1.5 was easiest to handle during cardiac operation and could be held in place with sutures. Use of rapidly bioresorbed film may be preferred to other materials in preventing the formation of a scaffold on which dense adhesions are formed.
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Fig 8. Before the sternum closure, the transparent film was placed on the surface of the heart with four corners slightly affixed to the pericardium.
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Acknowledgments
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We thank Daniel Cohn, PhD, Wefki Girgis, DVM, and Norma Roda, DVM, for their expert technical assistance. Dr Oz is an Irving Associate Professor at Columbia University.
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Footnotes
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This study was supported in part by Life Medical Sciences, Inc. Eli Pines is an employee of Life Medical Sciences, Inc, and has a stock holding position.
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References
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Accepted for publication March 18, 1999.
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Abstract
Introduction
