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Ann Thorac Surg 2002;73:1500-1506
© 2002 The Society of Thoracic Surgeons

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Original article: cardiovascular

BioGlue surgical adhesive impairs aortic growth and causes anastomotic strictures

^a The Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas, USA
^b Cullen Cardiovascular Research Laboratories, Texas Heart Institute, Houston, Texas, USA

* Address reprint requests to Dr LeMaire, 6560 Fannin St, Suite 1100, Houston, TX 77030 USA
e-mail: slemaire{at}bcm.tmc.edu

Presented at the Thirty-seventh Annual Meeting of The Society of Thoracic Surgeons, New Orleans, LA, Jan 29–31, 2001.

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. BioGlue surgical adhesive (CryoLife, Inc, Kennesaw, GA) is currently being used to secure hemostasis at cardiovascular anastomoses in adults. Interference with vessel growth would preclude its use during congenital heart surgery. The purpose of this study was to determine if BioGlue reinforcement of aortic anastomoses impairs vessel growth and causes strictures.

Methods. Ten 4-week-old piglets (8.0 ± 1.4 kg) underwent primary aorto-aortic anastomoses. Five piglets were randomly assigned to anastomotic reinforcement with BioGlue. After a 7-week growth period, the aortas were excised for morphometric analysis and histopathology.

Results. Weight gains were similar in both groups. In BioGlue animals, however, aortic circumference increased only 1.5 ± 0.8 mm (versus 2.7 ± 0.8 mm in controls; p = 0.054). BioGlue animals developed a 33.9% stenosis of the aortic lumen area (versus 3.7% in controls, p = 0.038). Adventitial changes reflecting tissue injury and fibrosis were present in all BioGlue animals versus none of the control animals (p = 0.008).

Conclusions. BioGlue reinforcement impairs vascular growth and causes stricture when applied circumferentially around an aorto-aortic anastomosis. This adhesive should not be used on cardiovascular anastomoses in pediatric patients.

	Introduction

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Bleeding complications during and after congenital heart operations remain a major source of morbidity and mortality. The repair of congenital heart defects in neonates and infants carries a particularly high risk of postoperative hemorrhage due to increases in hemodilution and inflammatory response during cardiopulmonary bypass, variable responses to heparin, multiple suture lines, and preoperative cyanosis with polycythemia [1]. Secondary complications—including coagulopathy, pulmonary artery hypertension, multiple organ failure, and transmission of infectious diseases—may result from the prolonged cardiopulmonary bypass times and increased transfusion requirements that are associated with perioperative bleeding. In an effort to reduce these complications, surgical adhesives and sealants have been used to improve hemostasis during congenital heart operations [2–5].

A new surgical adhesive composed of bovine albumin and glutaraldehyde (BioGlue; CryoLife, Inc, Kennesaw, GA) is currently being used in adults as an adjunct for securing hemostasis at cardiovascular anastomoses [6–9]. Compared with other currently available products, such as fibrin sealant, this adhesive has superior bonding and sealing capabilities. Broadening of clinical applications is inevitable and could include reinforcement of cardiovascular anastomoses during repair of congenital heart defects. Although the potential reduction of perioperative bleeding complications in children is attractive, no studies have evaluated the safety of BioGlue in this setting. Interference with vessel growth would preclude its use during congenital heart surgery. The purpose of this study was to determine if BioGlue reinforcement of aortic anastomoses impairs vessel growth and causes strictures.

	Material and methods

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The protocol was approved by the Institutional Animal Care and Use Committees at both Baylor College of Medicine and The Texas Heart Institute. All animals were fully examined by a staff veterinarian prior to operation and received humane care and handling in compliance with "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and "Guide for the Care and Use of Laboratory Animals" (NIH Publication no. 85-23, revised 1985).

Operative protocol
Ten 4-week-old domestic piglets (8.0 ± 1.4 kg) underwent general anesthesia. Arterial pressure was monitored through an 18-gauge catheter placed in the right carotid artery. Under sterile conditions, the infrarenal abdominal aorta was exposed through a midline laparotomy (transperitoneal approach). After intravenous heparin (3 mg/kg) was administered and allowed to circulate, clamps were placed on the aorta below the renal arteries and above the bifurcation. The aorta was transected at the midpoint between the renal arteries and the bifurcation. A 2-mm ring of aorta was excised from the proximal stump and split longitudinally to allow accurate measurement of the aortic circumference. An end-to-end aorto-aortic anastomosis was performed with interrupted 6-0 polypropylene sutures. Metallic clips were placed adjacent to the anastomosis for subsequent radiographic localization. After assuring hemostasis, aortography was performed to confirm patency. The aortogram was recorded using video cinefluoroscopy (OEC, Salt Lake City, UT) while injecting radiopaque contrast through a catheter placed in the aorta above the anastomosis. After completion of the anastomosis and aortogram, a sealed randomization envelope was opened and the piglet was assigned to either the BioGlue group or the control group; therefore, the surgeons were blinded to treatment group during performance of the anastomosis.

In animals assigned to the control group the anastomosis was left as is without the use of hemostatic adjuncts. In the other five piglets a layer of BioGlue was applied around the entire anastomosis. The adhesive was applied as per manufacturer instructions; the investigators (SAL, JSC) were trained by CryoLife, Inc, in the application of BioGlue and have experience in its clinical use during cardiovascular operations [6]. The BioGlue application device—including the preloaded cartridges, delivery gun, and mixing tips—were identical to those currently used in clinical practice. BioGlue has relatively poor viscosity. Therefore as the BioGlue spilled off the aorta during application, all excess adhesive was immediately removed with suction; every attempt was made to limit the final band of glue to the anastomotic site (Fig 1).

View larger version (133K): [in this window] [in a new window]   Fig 1. Intraoperative photograph of an aorto-aortic anastomosis in a 4-week-old piglet. The anastomosis is covered circumferentially with a thin band of BioGlue (arrow).

Histopathology and morphometrics
The infrarenal aorta was grossly divided into 2- to 3-mm cross-sections, beginning 1 cm above the anastomosis and extended inferiorly to 1 cm below the anastomosis. Histologic 5-micron sections were prepared using hematoxylin and eosin and Geske’s stains. A cardiovascular pathologist (FJC) who was blinded to the treatment group assignments evaluated the histopathology.

After completion of the histology, microscopic sections of the aorta were digitally scanned using a Leaf Lumina Digital Camera (Leaf Systems, Inc, Westboro, MA) and an Axiophot Light Microscope (Carl Zeiss, Inc, Thornwood, NY). The magnification for the morphometric study was 1.25 x 1.25 (objective x optivar lenses). These images were captured and saved using Adobe Photoshop 5.5 (Adobe Systems, Inc, San Jose, CA). Images were then exported to an image analysis software package (Optimas 6.5, Media Cybernetics, Silver Springs, MD) with macros specifically tailored to cardiovascular morphometrics. After calibration using a stage micrometer, microscopic images were analyzed with a specific macro designed to measure vessel circumference, area, and diameters. Sections of aorta at the anastomosis and 1 cm above the anastomosis were traced at specific borders—ie, the outer circumference and the endothelium—identified by the stain and structural morphology. Specific parameters measured included outer circumference, outer diameter, lumen diameter, and lumen area. Overall aortic area was the area within the outer wall circumference and lumen area was the area within the endothelium.

Aortic growth was assessed by calculating the changes in outer circumference and aortic area over the 7-week period. Anastomotic stenosis was evaluated by comparing measurements (aortic area, lumen diameter, and lumen area) between the proximal sections (P) and the anastomotic sections (A):

Statistical analysis
All data were entered into a database and analyzed using SPSS software (release 6.1.3; SPSS, Inc, Chicago, IL). Continuous data are expressed as mean ± standard deviation and were compared using t tests for independent samples. Categorical data were compared using the Fisher exact test (two-tailed). All p values less than 0.05 were considered statistically significant.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Aortography
Figures 2 and 3illustrate findings from aortography in control and BioGlue animals. All anastomoses were patent during the first operation. Aortography during the second operation confirmed patency of the anastomosis and distal aorta in 9 of the 10 animals. One pig in the BioGlue group had severe stenosis at the anastomosis during the first operation; the subsequent aortogram revealed progression of the stenosis and complete thrombosis immediately distal to the anastomoses. Morphometric data in this animal demonstrated no increase in circumference, a decrease in overall aortic area (-2.6 mm²), and 94.7% stenosis of lumen area. Because the thrombosis was caused by technical failure, these data are not attributable to the BioGlue; therefore this animal was excluded from further analysis.

View larger version (71K): [in this window] [in a new window]   Fig 2. Abdominal aortograms in an animal from the control group performed at (A) 4 weeks of age and (B) 11 weeks of age. The anastomosis is marked by the metallic clips. There is vessel spasm near the aortic clamp, but no obvious stricture at the anastomosis.

View larger version (69K): [in this window] [in a new window]   Fig 3. Abdominal aortograms in an animal from the BioGlue group performed at (A) 4 weeks of age and (B) 11 weeks of age. The anastomosis is marked by the metallic clips. There is vessel spasm near the aortic clamp and a focal stenosis at the anastomosis after the growth period.

View larger version (59K): [in this window] [in a new window]   Fig 4. (A) The histologic section from the aortic anastomosis in an animal from the control group demonstrates suture tracts (arrows) and a mild increase in adventitial connective tissue (bracket). (Geske’s stain, magnification 1.25 objective x 1.25 optivar). (B) The section from the anastomosis in an animal from the BioGlue group demonstrates more severe accumulation of adventitial connective tissue (bracket), dense infiltration by macrophages, and multiple micropyogranulomas (arrows). (Geske’s stain, magnification 1.25 objective x 1.25 optivar).

View larger version (119K): [in this window] [in a new window]   Fig 5. This histologic section from the aortic anastomosis in an animal from the BioGlue group demonstrates dystrophic mineralization (arrows) and eosinophilic islands of BioGlue (*) surrounded by dense adventitial inflammation and fibrosis (Geske’s stain, magnification x5).

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

BioGlue—a new surgical adhesive composed of 45% bovine albumin and 10% glutaraldehyde—has been developed as an adjunct to improve hemostasis during cardiovascular surgery. We and other authors currently advocate using BioGlue during repair of acute proximal aortic dissection in adults [6–9]. While we remain enthusiastic about using BioGlue as an adjunct in this setting, the glutaraldehyde component of this adhesive raises concerns regarding potential toxicities. We have recently demonstrated that contact between BioGlue and the phrenic nerve consistently causes acute nerve injury and paralysis of the diaphragm [10]. We have also demonstrated similar toxicities involving the cardiac conduction tissue [11].

Many cardiovascular operations performed in the pediatric setting involve primary vascular anastomoses that are required to enlarge as the patient grows. To be a safe and effective reinforcement for cardiovascular anastomoses in young patients, BioGlue must not interfere with future growth; the development of an anastomotic stenosis would produce hemodynamic complications and require additional intervention. Based on these concerns we designed this study to determine the effect that circumferential BioGlue reinforcement has on vessel growth by comparing aortic anastomoses in neonatal piglets randomized to undergo surgery with versus without the adhesive.

All four piglets in the BioGlue group had histologic evidence of severe fibrosis surrounding the aorta and involving the adventitia. This translated into impaired growth as measured by smaller increases in aortic circumference and area when compared with control animals. These differences in aortic growth approached statistical significance after only 7 weeks; a longer growth period would likely result in a wider discrepancy in aortic size. Furthermore, significant stenosis occurred at the anastomoses in the BioGlue animals regardless of the parameter measured (ie, outer diameter, lumen diameter, and lumen area). Although a concentric ring of hardened glue could contribute to the development of stenosis, the histologic evidence supports tissue injury and fibrosis as major factors in the impaired growth. Therefore, even localized, noncircumferential application to a growing vessel may result in stenosis. A similar study examining aortic growth after applying BioGlue to only a portion of the anastomosis would address this issue further.

The present data must be interpreted with the caveat that the tissue reaction to BioGlue may vary substantially depending on anatomic location, species, and age. Herget and associates [12] performed bronchial anastomoses with BioGlue in sheep. After 2 weeks, histology revealed localized tissue necrosis and an "inflammatory tissue response consisting of polymorphonuclear neutrophils, macrophages," and foreign body giant cells. Granulomatous changes persisted at 4 weeks but then improved by 12 weeks. Hewitt and associates [13] examined the descending thoracic aorta in sheep 3 months after application of BioGlue and noted "a relative paucity of prominent inflammatory response," other than rare examples of chronic granulomatous inflammation consistent with a typical foreign body response. Similarly, Gundry and colleagues [14] performed internal thoracic artery to coronary artery anastomoses in yearling goats and did not find any microscopic evidence of an inflammatory reaction 1 year after operation. Given the variability of tissue reactions, it is difficult to extrapolate our data to other settings such as adult vascular anastomoses. Further studies are needed to assess the clinical relevance of BioGlue-induced inflammatory changes.

Although it focuses on a more toxic adhesive, the recent report by Bingley and associates [5] provides an important opportunity for clinical correlation. Their report focused primarily on complications related to the use of gelatin-resorcinol-formaldehyde/glutaraldehyde glue (GRFG) in patients treated for acute proximal aortic dissection. Sixteen patients underwent aortic valve resuspension and aortic repair with GFRG glue; 6 of these patients (38%) required reoperation for aortic valve insufficiency. Reoperation revealed periadvetitial fibrosis, aortic tissue described as appearing "necrotic," and aortic redissection in the proximal ascending stump at the site where the adhesive was applied. Histology revealed dense acellular fibrosis, islands of hyaline material, and widespread hemosiderin deposition. More importantly, the authors reported serious late complications in 3 neonates in whom GRFG glue was used to reinforce anastomoses during arterial switch operations. One child died suddenly at home 1 month after surgery; autopsy revealed fibrosis involving the pulmonary artery and the coronary artery reattachment sites. The other 2 children required reoperation for marked pulmonary artery stenosis 1 month after the initial operation. The pulmonary arteries were "surrounded by very dense fibrous tissue." One child also had stenosis of the ascending aorta. One of the patients requiring reoperation died and the other underwent a third operation for continuing pulmonary artery stenosis. The similarities between the gross and histologic findings in Bingley and colleagues’ clinical report and the current porcine study—coupled with the glutaraldehyde component shared by GRFG glue and BioGlue—strengthens the argument that BioGlue is not well suited for use in congenital heart surgery. We agree with the authors’ recommendation regarding the use of tissue adhesives during congenital heart operations: if one is needed, fibrin sealant appears to be the safest option. Fibrin sealant has been used in pediatric heart surgery for more than 20 years [2–4]. Although interference with vessel growth has not been reported, an update of this extensive experience would help validate the recommendation.

In conclusion, circumferential BioGlue reinforcement of aorto-aortic anastomoses in piglets resulted in marked adventitial inflammation, fibrosis, impaired vascular growth, and stenosis of the lumen. Based on these results, further studies are needed to evaluate the safety of using this adhesive in growing vessels. Until then, BioGlue should not be used on cardiovascular anastomoses in pediatric patients.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
This study was funded entirely through the generous support of the Michael E. DeBakey Department of Surgery and the Division of Congenital Heart Surgery at Baylor College of Medicine. CryoLife, Inc. provided the surgical adhesive and delivery devices for this study and has provided research funding for other studies. The authors thank Cüneyt Köksoy, MD, for his technical assistance during the operations and Aimee Porter and Kathleen McKay for their superb anesthetic management.

	Appendix

 
DR MARK F. O’BRIEN (Brisbane, Australia): Bingley’s work that you quoted was done at our institution and we regarded, in our use of the GRF glue, that there was an excessive use of glue. As a result of that, we changed to BioGlue from the GRF. We have had the experience now in some 250 patients; a good proportion of those are pediatric and we have seen no problems.

My concern with your experimental work, as with our clinical experience with the GRF glue, was the excessive amount of glue that could be used that might produce perhaps an exaggerated stenosis or a failure of growth. We can use too much glue across an anastomosis, and I wonder what your comment is on that?

DR LEMAIRE: Thank you for your comments. The application of excessive glue could worsen the amount of fibrosis and the stricture just from the ring of hardened glue could be significant. We tried to limit application to a thin bead of glue—I think you could see this in the illustration—placed strictly around the area of anastomosis and typically used less than 2 cc of the product on this area. But certainly the application of more glue might cause more severe fibrosis and worsen the results.

DR WILLIAM D. SPOTNITZ (Philadelphia, PA): I want to congratulate you on this beautiful piece of work. More work on tissue adhesives will educate us how to use them properly and when not to use them. We certainly need instruction in this area.

I have a question for you related to the idea of whether this is a phenomenon that is like running a continuous suture around an anastomosis, which won’t allow the anastomosis to grow, as opposed to an interrupted suture anastomosis, which would? Or is there actually a process of active narrowing of the anastomosis as opposed to a lack of growth? Specifically, are we just seeing a prevention of growth or is there a further narrowing and shortening of the anastomosis created by the adhesive?

DR LEMAIRE: Thank you for your kind comments. That was certainly a consideration when we designed this study and was one of the reasons we used the interrupted sutures rather than a running suture. Without the histologic data, you could easily argue that it might just be the ring of hardened glue that is causing the problem. But the histologic data show extensive changes in the adventitia with micropyogranulomas, dense macrophage infiltrates, and a more severe degree of adventitial fibrosis than in the controls. This supports the idea that it is really a reaction to the glue that is causing the stenosis and not strictly a ring formation from the glue.

In the report by Bingley, the authors also described these marked inflammatory changes within the aortic specimens that they looked at.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Scott A. LeMaire Joseph S. Coselli Charles D. Fraser, Jr Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by LeMaire, S. A. Articles by Fraser, C. D. Search for Related Content PubMed PubMed Citation Articles by LeMaire, S. A. Articles by Fraser, C. D., Jr Related Collections Great vessels