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Ann Thorac Surg 2000;69:1764-1768
© 2000 The Society of Thoracic Surgeons

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Original articles: Cardiovascular

Late complications of tissue glues in aortic surgery

^a Department of Cardiothoracic Surgery, The Prince Charles Hospital, Chermside, Queensland, Australia

Address reprint requests to Dr Bingley, Department of Cardiothoracic Surgery, The Prince Charles Hospital, Chermside, Queensland 4032, Australia
e-mail: j.bingley{at}uq.net.au

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Tissue glues are used in cardiothoracic surgery as an adjunct to operative procedures where tissues are frail, as in aortic dissection, or where added hemostasis is required. This study was undertaken to review the use of tissue glue in our institution over a 5.5-year period. The aim of the study was to identify any potentially glue-related complications.

Methods. A review of tissue glue use for the period from January 1993 to September 1998 was performed and pre-, intra-, and postoperative parameters were collected. After some unusual surgical findings, of special interest was a range of pathology found at late reoperation.

Results. A total of 67 cases of tissue glue use were identified, with the majority of operations for type A dissection (76%). There were two intraoperative deaths. Twenty-seven of 65 patients (41%) required 29 further open chest operations; of these, 17 were for acute problems of bleeding or tamponade. Twelve patients (18%) underwent late reoperations months to years later. Nine of these patients, concentrated in two operative groups (7 patients with aortic valve resuspension and 2 patients who had undergone "switch" operations for transposition of great vessels), displayed complications related to the application of gelatin-resorcinol-formaldehyde (GRF) tissue glue.

Conclusions. Indications for tissue glues in cardiothoracic surgery must be carefully considered. We have reviewed our use of some tissue glues in acute type A aortic dissections and in pediatric cardiac patients and have discontinued the use of GRF glues because of unsatisfactory long-term complications.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Tissue glues, now a standard part of the armamentarium of the cardiothoracic surgeon, are useful in reinforcing fragile tissues in the treatment of acute aortic dissection and in assisting hemostasis and suture line support [1–4]. The use of tissue glues in repair of acute aortic dissection, in particular the gelatin-resorcinol-formaldehyde glues, has been reported to reduce mortality significantly from this surgical emergency [4].

Although several glues are available to the cardiac surgeon at present, gelatin-resorcinol-formaldehyde/glutaraldehyde glues have become the standard choice in assisting repair of type A dissections [3, 5]. This adhesive combination, popularized by French cardiothoracic surgeons in the late 1970s for treatment of acute type A aortic dissections (hence called "French" glue), produces a waterproof lattice of macromolecules when combined, and displays excellent adhesive properties [6, 7]. Other glues, including fibrin glues [8] and acrylates [9], have been employed in acute type A aortic dissections. New biological adhesive combinations continue to appear (eg, Bioglue, 45% bovine serum albumin and 10% glutaraldehyde; Cryolife International Inc, Kennesaw, GA), offering the surgeon several alternatives from which to choose in aortic dissection repair.

The method of application of tissue glue has been well reported, both in company literature and medical literature [6, 7, 10] (GRF; Fabrique d’Implants et d’Instruments Chirurgicaux, Saint-Just-Malmont, France and Bioglue; Cryolife International Inc). Although there are continued questions about the potential clinical, toxic, and carcinogenic effects of the formaldehyde component [7, 11], in general, GRF glue has been held to be a safe product. In this paper, we highlight our concerns with the late effects of GRF glue after acute type A repair that involved resuspension of an incompetent aortic valve, particularly in the high incidence of abnormal macroscopic morphological findings noted at the time of late or delayed reoperation. We also report adverse outcomes from GRF glue in a small number of pediatric patients.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
This study was undertaken to review our institution’s recent experience with tissue glues in cardiac surgery in light of anecdotal reports of unusual findings in cases of reoperation where tissue glues had been previously employed. A retrospective review of the use of tissue glue at the Prince Charles Hospital, Brisbane, Australia was performed covering the period 1993 to 1998. Patients were identified through hospital database records. Information collected included patient demographic data (age, gender, preoperative comorbidities), indications for surgery, pathology found at surgery, details of operative techniques including the site of application and type of tissue glue used, course of postoperative recovery, and complications including the necessity for reoperation. In those patients who underwent reoperation, the indications for and findings at surgery were noted. Where specimens of glue-affected tissue were taken, histological analysis was performed and findings were noted.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Sixty-seven patients were identified in whom tissue glues had been used in the course of their cardiac surgery (46 males and 21 females with a mean age was 58 years). Most patients had at least one comorbid condition: aortic regurgitation, 35; hypertension, 31; renal insufficiency (creatinine > 130 mg/L), 22; ischemic heart disease, 11; pulmonary disease, 11; limb ischemia, 11; central nervous system changes, 6; Marfan’s disease, 6. Fifty-eight patients presented as emergencies, and the remaining 9 patients undertook elective procedures. Surgical access was almost exclusively via a median sternotomy. At surgery, the pathological findings were varied, although the majority of patients had acute type I aortic dissection (76%): type A aortic dissection, 51; annulo-aortic ectasia, 7; homograft failure, 2; transposition of great vessels, 3; ventricular rupture, 1; aortic root abscess, 1; traumatic aortic rupture, 1; pseudo-aneurysm (previous Bentall), 1. In these patients, the underlying pathology was typically cystic medial degeneration or atherosclerosis. In 3 patients, the aortic dissection closely followed elective surgery for coronary artery disease (2 patients) or aortic valve surgery (1 patient).

GRF tissue glue was the most commonly used tissue glue (59 of 67 [88%]). In three cases, fibrin glue was used. More recently, a biological glue consisting of 45% bovine serum albumin and 10% glutaraldehyde (Bioglue) has been employed (5 patients). In patients with acute type A aortic dissection, one of three glue types were utilized in reinforcement of the dissected proximal and distal ends of aorta: GRF in 49 cases, and Bioglue and fibrin in one case each. Where resuspension of the aortic valves was necessary, Teflon felt pledgets were used for support. Tissue glues were used for reinforcement of anastomoses and hemostatic control in the remaining patients. In these operations, GRF glue was again the most commonly used (10 patients), whereas fibrin glue has occasionally been used in past years (2 patients), and in recent months, Bioglue has been used (4 patients).

Mean follow-up for the cohort (excluding in-hospital mortalities) was 22 months, with 4 patients lost to follow-up. There were two intraoperative deaths. A further 9 patients died in hospital at a mean of 9.7 days after surgery. Overall in-hospital mortality rate for surgery in which tissue glues were used was 17%. Of the 65 patients who survived initial operation, 38 required no further surgical intervention. Twenty-seven patients (39%) were returned to the operating theater for a total of 29 operations at some time after the initial operation. Seventeen of these acute operations were for control of hemorrhage or treatment of tamponade within the first 3 weeks after initial surgery. Twelve patients returned for late operation at various times beyond the first 3 weeks (Fig 1). The mean delay to reoperation in this group was 40 months.

View larger version (24K): [in this window] [in a new window]   Fig 1. Distribution of late reoperations in patients after tissue glue use in cardiothoracic surgery.

In the subgroup with acute type A aortic dissections, 26 patients (51% of all type A dissections) had associated aortic valve insufficiency. Of these 26 patients, 8 progressed directly to successful combined aortic valve and aortic root replacement. The other 18 patients with type A dissections and associated aortic valve insufficiency had resuspension of the aortic valve performed at their first operation. One of these latter patients died in hospital after initial repair. Of the 18 patients with resuspension of their aortic valves, 8 returned for delayed reoperation, 7 for aortic regurgitation (39% of valve resuspensions), and 1 for dissection of their descending thoracic aneurysm.

Late reoperations
The patients who returned for late reoperation represent the focus for this review. In total, there were 10 adults and 2 infants in this late reoperation group. Initial surgery in 8 patients was as an emergency for acute type A aortic dissection, with use made of GRF glue to restore integrity to the dissected aortic cuffs at the proximal and distal anastomotic sites and aortic valve resuspension. One patient returning for late operation after aortic valve resuspension in acute type A aortic dissection required replacement of a descending thoracic aneurysm at 12 months after initial surgery. The remaining 7 patients returned for late reoperations with aortic regurgitation at a mean of 35 months (range 22 to 48 months) after initial aortic valve resuspension. In 6 of these 7 patients, the aorta had redissected at the site of previous GRF glue use in the proximal aortic root with associated aortic valve incompetence, suggesting the glue had failed to assist the operative resuspension or the glue was not used appropriately. An unusual appearance of the redissected aortic root intimal tissue was found. The operation reports contain various descriptive terms ("degeneration," "blackened," or "necrotic"), which suggest some form of chronic degradative process occurred. Histology of the redissected intima revealed a nonspecific dense acellular fibrous tissue with islands of hyaline material and widespread hemosiderin deposition (Fig 2). Two adults whose initial surgery was not for acute type A aortic dissection also returned for surgery at later time points: 1 patient returned for debridement of sternal sequestra after aortic valve-conduit replacement in which GRF glue was used to support suture lines, and a second patient returned with a false aneurysm where fibrin glue was used for hemostasis in a homograft aortic valve/root replacement.

View larger version (138K): [in this window] [in a new window]   Fig 2. Photomicrograph showing redissected ascending aorta at site of GRF glue use consisting of dense acellular fibrous tissue with islands of hyaline material and widespread hemosiderin deposition (x200).

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
We have identified a concern with a number of our patients in whom tissue glues were used as part of their aortic surgery. Especially worrying have been those patients in whom GRF glue was used in the repair of type A aortic dissection with associated aortic valve regurgitation, and in pediatric patients. Tissue glues have several uses in cardiovascular surgery, including hemostasis, anastomotic support, and reinforcing frail tissues [2, 4, 12]. The use of GRF glues in restoring integrity to the aortic wall in acute type A aortic dissections was popularized by French surgeons in the late 1970s and has since been championed as a safe technique with good long-term outcomes [1, 4, 13]. Fibrin glues are more commonly promoted for hemostatic control, but have also been used safely for repair of type A aortic dissections [2, 14, 15]. Tissue glues are thus considered safe and useful adjuncts to several cardiac surgical procedures. Although this review of glue use within our institution encompassed all tissue glues used for a variety of pathological entities over a 5.5-year period, patients with type A dissection comprise the majority of patients in our study, and GRF glue was the major tissue glue used. The demographics of the cohort closely resemble published studies on glue use in type A aortic dissections in terms of mean age, gender distribution, associated comorbidities, postoperative complications, and 30-day mortality [1, 4, 13]. In-hospital mortality rate of 17% compares favorably with other studies [13, 15]. Reoperation rate after discharge, especially for type A dissections (16%), is identical to that of other studies [13].

Within the 5.5-year period, 12 of 65 patients surviving operation returned for reoperation after a delay of at least 1 month from the time of initial glue use; 9 of the patients demonstrated pathology at sites where tissue glue was previously used. In all but 1 of these late reoperation patients, GRF tissue glue was used. At reoperation some months to years after the initial use of GRF glue, two features stood out: tissues were heavily fibrosed at the site of glue application, and a number of patients had experienced redissection of the aortic root where GRF glue had been applied.

In our series, we found two groups of patients in whom tissue glues were used and subsequent glue-related problems were identified. First, neonates undergoing repair of transposition of the great vessels demonstrated clinical complications within 1 month after glue use (glue had not been used before 1998 for any neonatal surgery). Second, adults undergoing aortic valve resuspension for aortic regurgitation associated with acute type A dissection developed late aortic regurgitation (mean 35 months) after glue use.

Several groups have reported the safe use of glues in repair of acute type A aortic dissection. Most of these have used GRF [3, 4, 15], although some have advocated the use of fibrin glues [8]. GRF glues were initially advocated to reduce operative and postoperative mortality associated with acute type A aortic dissection, reducing in-hospital mortality to around 10% [1], although subsequent review by this group reports in-hospital mortality of around 21% [4] and the benefit in terms of mortality reduction remains contentious [16].

The long-term results of glue use as an adjunct to aortic valve resuspension for incompetence after acute type A dissection vary. Some authors report very low rates of recurrence of aortic incompetence (3% [13]), whereas others report moderately higher rates (20% [3] and 24% [4]). In the United States, where GRF glues are not used, resuspension of the aortic valve commissures for incompetence associated with acute type A dissection is often assisted by incorporation of a Teflon felt strip between the dissected intima and outer media to provide the adequate tissue strength. Excellent results have been reported for the long-term durability of this type of glue-free repair (100% and 80% at 5 and 10 years, respectively [17]). In contrast Simon and associates [18] report a high incidence of sinus of Valsalva aneurysm after repair of the ascending aorta without glue, and altered their repair technique to include resorcinol glue. They are yet to report on their experience with GRF glues although they do report improved short-term results in this group using a David technique of aortic root replacement to preserve aortic valve function [19].

Our study has an alarmingly high rate of late aortic valve incompetence (7 of 18 patients [39%]) for patients in whom the dissected aortic root was reinforced with GRF glue to aid aortic valve resuspension where valve preservation was attempted. In 6 patients, the aortic root was noted to have redissected at the site of glue application, and the morphology of the new intimal flap was unusual both macroscopically and microscopically. These findings are consistent with recent reports of glue repair failure showing similar high rates of reoperation for redissection after local repair in acute ascending aortic dissection [20, 21].

There are several possibilities that might explain this result. First, the glue may have been applied incorrectly. Much is written on the need to apply GRF glues in an appropriate manner, ensuring tissues are dry and the intimal flap is reapposed under pressure to ensure proper bonding [4, 13]. The surgeons involved are cognizant of these requirements and all attempts are made to follow these steps, as well as manufacturers’ guidelines for glue use. There are some practical limitations to the delivery of the GRF glue in its current presentation, especially with the accurate application of the formaldehyde/glutaraldehyde polymerization solution. Formaldehyde has a potential necrotic action on tissues, and a delivery system where spillage is possible is less than acceptable.

A further possible explanation is that the glue has failed despite appropriate use, through an intrinsic fault within the glue itself or its effects on the tissues to which it is applied. Certainly, the tissue appearance is unusual at reoperation, and the intimal flap’s abnormal microscopic appearance together with its degenerate appearance and associated periadventitial fibrosis may result from tissue damage due to one or more of the glue’s components. The use of GRF glue in the neonatal cases was unwise, and the data are included here to caution others from using similar glues in such cases. If a tissue glue is required for hemostasis, a fibrin glue should be selected.

We have presently discontinued our use of GRF glue as a result of this review. Clearly, GRF glue must be used with extreme caution on maturing vascular structures, and we will not use it in neonates again. We are changing our management of acute type A aortic dissections and will be more cautious in using tissue glues to support the aortic wall, especially where the aortic valve is to be resuspended. It remains to be tested whether alternative methods provide better management of these and other conditions.

	References

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				R. G. Leyh, S. Fischer, K. Kallenbach, T. Kofidis, K. Pethig, W. Harringer, and A. Haverich High Failure Rate After Valve-sparing Aortic Root Replacement Using the "Remodeling Technique" in Acute Type A Aortic Dissection Circulation, September 24, 2002; 106(12_suppl_1): I-229 - I-233. [Abstract] [Full Text] [PDF]

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				M. Ueno, T. Imada, K. Nonaka, and T. Oda Aortopulmonary fistula after aortic root replacement Ann. Thorac. Surg., August 1, 2002; 74(2): 590 - 591. [Abstract] [Full Text] [PDF]

				K. Lachapelle, B. deVarennes, P. L. Ergina, and R. Cecere Sutureless patch technique for postinfarction left ventricular rupture Ann. Thorac. Surg., July 1, 2002; 74(1): 96 - 101. [Abstract] [Full Text] [PDF]

				S. A. LeMaire, Z. C. Schmittling, J. S. Coselli, A. Undar, B. A. Deady, F. J. Clubb Jr, and C. D. Fraser Jr BioGlue surgical adhesive impairs aortic growth and causes anastomotic strictures Ann. Thorac. Surg., May 1, 2002; 73(5): 1500 - 1506. [Abstract] [Full Text] [PDF]

				M. Ceviz, Y. Unlu, and N. Bect Aortic arch replacement in acute aortic dissection J. Thorac. Cardiovasc. Surg., March 1, 2002; 123(3): 586 - 587. [Full Text] [PDF]

M. Kirsch, M. Ginat, L. Lecerf, R. Houel, and D. Loisance Aortic wall alterations after use of gelatin-resorcinol-formalin glue Ann. Thorac. Surg., February 1, 2002;