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Ann Thorac Surg 2007;83:1621-1626
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Late Complications of Gelatin-Resorcin-Formalin Glue in the Repair of Acute Type A Aortic Dissection

Hiroki Hata, MD, PhDa, Hiroshi Takano, MD, PhDa, Goro Matsumiya, MD, PhDa, Norihide Fukushima, MD, PhDa, Naomasa Kawaguchi, PhDb, Yoshiki Sawa, MD, PhDa,*

a Division of Cardiovascular Surgery, Department of Surgery, Osaka University Graduate School of Medicine, Osaka, Japan
b Department of Molecular Pathology, School of Allied Health Science, Osaka University Graduate School of Medicine, Osaka, Japan

Accepted for publication January 15, 2007.

* Address correspondence to Dr Sawa, Division of Cardiovascular Surgery, Department of Surgery, Osaka University Graduate School of Medicine, 2-2-E1, Yamadaoka, Suita, Osaka, 565-0871, Japan (Email: sawa{at}surg1.med.osaka-u.ac.jp).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: During surgical treatment for acute type A aortic dissection, gelatin-resorcin-formalin glue is generally applied and its efficacy has been reported. However, some late complications that are potentially associated with this glue have also been reported. In the present study, we reviewed our experiences of treatment for acute type A aortic dissection and late complications that occurred in the anastomotic site, which needed a reoperation.

Methods: From October 1994 to August 2005, 68 patients underwent emergency surgery for acute type A aortic dissection. Gelatin-resorcin-formalin glue was applied to 56 (82.4%) of these patients at one or both of the distal and proximal anastomosis sites.

Results: Eight (11.8%) patients died in hospital within 30 days after the operation, among which two patients already had cerebral complications prior to the surgery. There were five late deaths from causes unrelated to cardiac events. Five patients developed an aortic pseudoaneurysm at the anastomotic site and underwent a late reoperation. All of these patients had been treated with gelatin-resorcin-formalin glue during the previous operation. Histologic examination of the resected aortic wall after the reoperation revealed tissue necrosis, severe local inflammation, and organization of old thrombi at the site of the glue application.

Conclusions: Late complications after the use of gelatin-resorcin-formalin glue may occur with a certain amount of risk, suggesting its toxicity for aortic tissue. Therefore, proper use of this glue and close follow-up of the patients are strictly required.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Despite recent advances in surgical techniques and perioperative care, acute type A aortic dissection still remains a life-threatening disease with an in-hospital mortality rate of about 15% to 30% [1–3]. Emergency surgical treatment aimed at preventing aortic rupture into the pericardium or mediastinum and progression of the dissection process is indispensable for saving life. Because reinforcement of the fragile aortic wall and prevention of blood leakage at the anastomotic site are major concerns during the surgical treatment, various techniques, such as utilization of a Teflon felt (Meadox Medical Inc, Oakland, NJ) strip [4, 5], have been developed to address these problems.

Since gelatin-resorcin-formalin (GRF) glue was first introduced by Guilmet and colleagues in 1979 [6], it has generally been applied to strengthen the dissected layers of the distal and proximal aortic stumps and many reports have demonstrated its efficacy in reducing the operative mortality [7–9]. However, several late complications, such as redissection of the aorta, aortic pseudoaneurysm, and insufficiency of the aortic valve, have recently been suggested to be associated with treatment for acute type A aortic dissection using some types of biologic glue, especially GRF glue [10–15].

In our institution, we have used GRF glue since 1996, and some cases of late aortic pseudoaneurysm at the anastomosis site have been observed to date. In the present study, we reviewed the results of surgical treatment for acute type A aortic dissection and analyzed the causal relationship between the use of GRF glue and late complications originating in the anastomotic site, which needed a reoperation.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
From October 1994 to August 2005, 68 consecutive patients underwent emergency aortic replacement for acute type A aortic dissection in our hospital. There were 39 men and 29 women, with a mean age of 63.1 years (range, 27 to 88 years). Three (4.4%) patients had Marfan syndrome. According to the DeBakey classification, 43 (63.2%) patients were type I, 15 (22.1%) were type II, and 10 (14.7%) were type III with retrograde dissection. Aortic regurgitation was seen in 17 (25.0%) patients with trivial to mild grades and in 12 (17.6%) patients with moderate to severe grades. Two patients had undergone previous aortic valve replacement. Regarding the preoperative hemodynamic conditions, seven patients showed cardiac tamponade, including one patient with cardiogenic shock status, and 10 patients showed organ malperfusion, including three patients with cerebrovascular ischemia. This study received approval from the Institutional Review Board in Osaka University.

Operative Techniques
Prior to a median sternotomy, the femoral artery was cannulated, or a femoro-femoral circulatory bypass was established if the preoperative hemodynamic conditions were unstable. An 8-mm woven Hemashield graft (Boston Scientific, Natick, MA) was anastomosed to the side of the right axillary artery while a median sternotomy was carried out. Cardiopulmonary bypass was initiated after cannulation of the right atrium and core cooling was started. When the rectal temperature reached 20°C, the systemic flow was stopped and the ascending aorta was transected, opened longitudinally, and resected with the segment including the primary intimal tear. Additional antegrade selective cerebral perfusion (SCP) was used for brain protection if necessary. Next, GRF glue was employed in the distal false lumen by direct infusion of warmed gelatin-resorcin mixture between the two dissected walls, followed by placement of two or three drops of formalin using a 23G needle. The aortic stump was then gently compressed with clips for approximately two minutes. The glued distal stump was anastomosed with a woven Hemashield graft reinforced by a Teflon felt strip around the anastomotic site. In some cases, a bovine or equine pericardium strip was used to reinforce the anastomosis and GRF glue was applied between the strip and the adventitia. Antegrade arterial circulation was then resumed. Reconstruction of the aortic arch branches was performed in cases of total arch replacement. Aortic valve resuspension was performed when necessary. The GRF glue was also applied to the proximal stump and a proximal anastomosis was performed in the same manner as described above for the distal site.

According to the above strategy, prosthetic graft replacement of the ascending aorta was performed in all 68 patients. The basic operative technique has not changed for 11 years though there were three surgeons during that period. Extended treatments included hemiarch replacement (14 patients, 20.6%), total arch replacement (12 patients, 17.6%), and aortic root replacement using a composite graft (2 patients, 2.9%). Aortic valve resuspension was performed in 36 (52.9%) patients. Open distal anastomosis was performed under deep hypothermic circulatory arrest (DHCA) in 32 (47.1%) patients and antegrade SCP was performed in 36 (52.9%) patients for cerebral protection. The GRF glue was applied to obliterate the false lumen and reinforce the anastomotic sites in 56 (82.4%) patients at one or both of the distal and proximal anastomosis sites.

The patients were followed up until October 2005. The mean follow-up period was 56.9 months (range, 2 to 133 months). The routine follow-up was achieved by semiannual chest computerized tomography (CT) or magnetic resonance imaging (MRI).

Statistical Analysis
Values are expressed as the mean ± SD. Actuarial survival and freedom from reoperation were estimated by the Kaplan-Meier method.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Operative Mortality and Morbidity
The overall in-hospital mortality was 11.8% (8 of 68 patients). Two patients died from brain death, of which one required preoperative cardiopulmonary resuscitation and the other showed a preoperative severe brain injury with a central neurologic deficit. Other causes of in-hospital death were myocardial infarction in one patient, cerebral infarction in one, pulmonary embolism in one, low cardiac output in one, retroperitoneal hemorrhage in one, and sudden death of unknown cause in one. Postoperative paraplegia was seen in one patient. A postoperative hemorrhage requiring a rethoracotomy developed in seven patients. New central neurological deficits were observed in five patients postoperatively. Mediastinitis requiring transposition of the omental flap was observed in two patients.

Late Results
Late postoperative death was observed in five cases, none of which resulted from cardiovascular disease but chronic diseases such as leukemia, cerebral infarction, and cancer of digestive organs. The actuarial survival rates at one, three, and five years after the operation, including in-hospital mortality, were 83.4%, 81.4%, and 78.9%, respectively (Fig 1).


Figure 1
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  		Fig 1. Actuarial survival curve including hospital mortality.

 
A pseudoaneurysm developed at the anastomotic site in five (7.4%) patients and a late reoperation was required in all cases. In all five of these patients, GRF glue was used during the initial aortic operation. In contrast, no pseudoaneurysms were observed in any of the patients treated without GRF glue. The rates of actuarial freedom from reoperation relative to a pseudoaneurysm at the anastomotic site were 100% at one year after the operation, 93.4% at three years, 90.0% at five years, and 83.1% at seven years (Fig 2).


Figure 2
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  		Fig 2. Actuarial freedom from reoperation curve of all patients and the patients received gelatin-resorcin-formalin (GRF) repairs. (— = total; - - - = GRF (+).)

 
Pseudoaneurysms at the Anastomotic Site
The profiles of the five patients who underwent a late reoperation due to an aortic pseudoaneurysm at the anastomotic site are shown in Table 1. The initial postoperative course was satisfactory in each case. The pseudoaneurysms were identified by chest X-ray, chest CT, or MRI performed as a periodical inspection after the patients had left the hospital (Fig 3). The mean interval between the initial operation and the detection of a pseudoaneurysm was 36.0 months (range, 13 to 76 months). In all cases, both the proximal and distal aortic stumps had been reinforced by applying GRF glue. Moreover, in patients 3 and 4 the glue was also applied between the adventitia and a bovine or equine pericardium strip placed over the adventitia to reinforce the anastomosis.


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  		Table 1 Profile of Patients Who Developed an Aortic Pseudoaneurysm after Repair of Acute Type A Aortic Dissection Using GRF Glue
 

Figure 3
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  		Fig 3. Sagittal section view of a preoperative cineangiogram (A) and magnetic resonance imaging study (B) in patient 3, revealing a pseudoaneurysm (arrows) that originates from the proximal anastomosis site and is connected with the distal anastomosis site, forming a tunnel behind the prosthetic graft (arrowheads).

 
At the reoperation, a sternal reentry was performed uneventfully after femoral artery cannulation. Extracorporeal circulation was established with venous cannulation to the right atrium and DHCA was employed after core cooling. The pseudoaneurysm was opened and the previous graft was found to have partially detached from the aortic stump in all cases (Fig 4). The pseudoaneurysm was removed together with the previous prosthetic graft and the aorta was replaced with a new graft. In one patient, aortic root replacement was performed because aortic valvular annulus was intact though necrosis of the aortic wall had reached to the sinotubular junction. Another two patients underwent total arch replacement because of extension of pseudoaneurysm to the aortic arch.


Figure 4
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  		Fig 4. Intraoperative photography of patient 3. The ascending aorta and prosthetic graft were longitudinally opened. At both the anastomotic sites, the prosthetic graft has partially detached from the aorta. A tunnel is formed with the pseudoaneurysm behind the prosthetic graft. A pair of thoracic forceps is passed through the pseudoaneurysm tunnel. The outer wall of the pseudoaneurysm consists of surrounding connective tissues, the left atrium, and the pulmonary artery.

 
Macroscopically, the detached aortic stumps did not appear to be blackened or degenerative. Histologic examination of the resected aortic wall at the proximal anastomotic site, where the GRF glue was previously employed, revealed disruption of the intima and media in which the nuclei of the smooth muscle cells had mostly disappeared, suggesting necrosis. Hyaline degeneration and fibrinoid degeneration were also observed, indicating a healing process for the necrosis, as well as severe local inflammation with macrophage aggregates engulfing waste tissues and organization of old thrombi (Fig 5). No recurrence of pseudoaneurysm has been seen in the five patients to this day.


Figure 5
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  		Fig 5. Photomicrographs of a longitudinal section of the proximal anastomosis in patient 3 showing disruption and necrosis of the intima and media (arrowheads). Hyaline degeneration and fibrinoid degeneration, as well as local inflammation with macrophage aggregates engulfing the waste tissues (arrows), are observed at the anastomotic site. (A) Hematoxylin and eosin staining. (B), (C) Masson trichrome staining. Original magnification: x40 (A, B), x400 (C). (BP = bovine pericardium strip.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
In the present study, we have reported the early and midterm results of surgery for acute type A aortic dissection and we have also described some cases of aortic pseudoaneurysm formation requiring a reoperation in patients treated with GRF glue.

Despite recent advances in diagnosis, in surgical techniques, and in perioperative management, the operative mortality of acute type A aortic dissection remains high [1–3]. To improve this mortality, bleeding from fragile dissected aortic tissues is one of the major concerns that need to be managed at surgery. Reinforcement using Teflon felt has conventionally been used, as well as tissue glues. The use of tissue glues, particularly GRF glue, was initially reported to reduce early surgical complications and improve long-term survival rates after repair of acute aortic dissection [7–9]. Regarding the reoperation rates, Casselman and colleagues [16] reported that the incidences of aortic root reoperation were 11%, 23%, and 40% when GRF glue, Teflon felt, and fibrinous glue, respectively, were used for root reconstruction.

However, Fukunaga [10] and colleagues reported that GRF glue had no impact on the incidence of reoperation, while other articles commented that the benefits of GRF glue in terms of mortality reduction remain contentious [11, 17]. In addition, it was reported that approximately 10% to 20% of patients who underwent repair of acute type A aortic dissection using GRF glue developed aortic redissection, aortic pseudoaneurysm, and recurrence of aortic insufficiency and required a late reoperation, suggesting a close relationship between such late complications and the use of GRF glue [10–15]. In our institution, a postoperative aortic pseudoaneurysm at the anastomosis site was observed in 5 of 56 patients after the use of GRF glue, whereas no late complications were observed in patients treated without GRF glue. We consider that this result may support the relationship between late complications and the use of GRF glue, although our study had some limitations in that it was neither a randomized nor a comparative study.

The speculated causes of a late aortic pseudoaneurysm or redissection are either incorrect application of the GRF glue or toxic effects of the formalin. Inadequate mixing of the glue components, incomplete drying of the false lumen,, or insufficient pressure to attach the dissected aortic layers may lead to poor bonding and subsequent aortic pseudoaneurysm or redissection. Regarding the toxicity of GRF glue, some researchers have demonstrated the toxic effects of formalin and the possibility of causing tissue necrosis and have recommended avoiding formalin overdose [7, 18, 19].

The toxicity of formalin has also been supported histologically. In several reports, medial degeneration including disappearance of the nuclei in medial smooth muscle cells, hemosiderin deposition, and disruption of the medial elastic lamellae were observed, suggesting tissue necrosis [10–12, 20]. In our study, interruption of the intima and media with disappearance of the nuclei in smooth muscle cells, hyaline degeneration, and fibrinoid degeneration, which suggest tissue necrosis and a healing process of necrosis, were identified.

To obtain satisfactory effects using GRF glue and to reduce late complications, proper use of the glue, including the avoidance of formalin overdose, is indispensable. In addition, some contrivances for the application of the glue, such as using a finer needle when dropping the formalin, applying slightly hardened GRF glue mixed beforehand on a back table, and invaginating the adventitia inside the aortic lumen to contain the glue inside of the false lumen [21], have been introduced.

Another competing strategy is to use alternative glues. However, each of these glues has its own merits and demerits. For example, BioGlue (Cryolife, Kennesaw, GA), which was approved by the US Food and Drug Administration unlike the case for GRF glue, was thought to be less histotoxic with superior bonding and sealing capabilities, and has been widely applied [22, 23]. However, Furst and colleagues [24] demonstrated in vitro and in vivo toxicities of glutaraldehyde released from BioGlue and Hoschtitzky and colleagues [25] indicated that BioGlue was more liquid and potentially more likely to reach the vessel lumen and cause an embolism than GRF glue. Furthermore, Kazui and colleagues [26] reported pseudoaneurysm formation in two of five patients treated with BioGlue. A fibrin sealant is thought to be more effective in controlling bleeding than GRF glue. However, GRF glue can produce a significantly greater tensile strength than a fibrin sealant [27].

In response to our review, we have recently reduced the number of cases of acute type A aortic dissection treated with GRF glue in our institution. On the occasion of its application, we pay close attention not to drop excessive amounts of formalin or spill it over the surrounding tissues, and to only apply two or three drops of the formalin using a 23G needle.

In conclusion, our recent experience of surgical treatment for acute type A aortic dissection demonstrated satisfactory early and late mortality. However, we also found some late aortic pseudoaneurysms requiring a reoperation only in patients treated with GRF glue during the operation. A pathohistologic study suggested that the occurrence of aortic pseudoaneurysm at the anastomosis site was possibly caused by the toxicity of the GRF glue. Therefore, indications for the use of GRF glue must be meticulously considered and, on the occasion of its employment, an appropriate technique and administration of a proper amount of GRF glue, especially formalin, are strictly required. Furthermore, it is very important to remember that late complications may occur after the use of GRF glue in the repair of acute type A aortic dissection and to follow up outpatients closely.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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