An Observational Study of Bovine Pericardial Patch Angioplasty as a surgical option for Infected Aortic Aneurysms

Background: An infected aortic aneurysm (IAA) is a rare and life-threatening disease. The aim of this study is to elucidate mid-term outcomes of IAA, incorporating patch angioplasty with bovine pericardium. Materials and Methods: Between June 2011 and August 2020, eight patients (one woman, seven men) with infected aneurysms of the thoracic and abdominal aorta were treated surgically. Results: There was no surgical/hospital death. There were two late deaths at follow-up. One patient (patient 6) was re-admitted to the hospital with vomiting blood four months after surgery and died despite treatment. Another patient (patient 5) died at his home 12 months after surgery, and the cause of death was unknown. Six patients remained alive with no evidence of recurrent aneurysm formation due to infection at a mean follow-up of 70.3 (range, 13-110) months. Conclusions: BPPA could be one of the surgical options for IAA, especially in patients with severe adhesion around the aneurysm.


Introduction
An infected aortic aneurysm (IAA) is a rare and life-threatening disease [1,2]. Surgical treatment for IAA is difficult and the ideal surgical procedure and optimal graft material remain subjects of debate [3]. Bovine pericardial patches (BPPs) are used in the infected fields [4,5,6]. In view of the anatomic characteristic of saccular form in IAAs, we completed a patch repair of the aortic intima defect using a BPP. Bovine pericardial patch angioplasty (BPPA) has low invasiveness because it minimizes the dissection range around the aneurysm, and handling of bovine pericardium is easy, which may shorten the operative time, hence potentially beneficial in clinical outcome [3,7,8]. The aim of this study is to elucidate mid-term outcomes of IAA, incorporating patch angioplasty with bovine pericardium.

Materials and Methods
Between June 2011 and August 2020, eight patients (one woman, seven men) were diagnosed with infected aneurysms of the thoracic and abdominal aorta. Age at operation range from 60 to 86, average 75 years. Patients with an infected aneurysm after previous vascular surgery, or a prosthetic graft infection, or those with aortoduodenal fistulas without previously infected aneurysm, were excluded from the study (Table 1).

Table 1. Patient profiles
The diagnosis of IAA was confirmed based on a combination of clinical symptoms and signs of infection, results of laboratory tests (white blood cell count and C-reactive protein levels), and typical imaging study findings (saccular aneurysm, para-aortic soft tissue infiltration, and abnormal fluid accumulation around the aneurysm; Figure 1) [9]. In some cases, 18F-fluorodeoxyglucose (FDG)-positron emission tomography (PET)/CT was used to confirm the diagnosis ( Figure 2). Once the diagnosis of primary IAA was established, intravenous broadspectrum antibiotics were administrated empirically. A most appropriate antibiotic was determined after culture results and sensitivity reports were available. All patients received intravenous antibiotic treatment for at least 4 weeks or until their body temperature, white blood cell count, and C-reactive protein levels turn to normal. After discharge, oral antibiotic treatment was continued for at least 6 to 11 months Of the eight patients, the infrarenal abdominal aorta was involved in four patients, and the thoracoabdominal aorta, and juxtarenal aorta in two each. A rupture was found in four of the 8 patients, including an aortic sigmoid colon fistula in one. Six patients were performed through midline abdominal approach and two patients through thoracoabdominal approach. Severe adhesion around the aneurysm was observed in all cases. Partial cardiopulmonary bypass and selective visceral artery perfusion was used in two patients with infected thoracoabdominal aortic aneurysm ( Figure 3). The aneurysm of the thoracoabdominal aorta was markedly expanded. Severe adhesion around the aneurysm was observed. B: Distal descending thoracic aorta (Th 8) and the aorta just above the left renal artery between the Th12 and L1 were cross-clamped. Superior mesenteric artery (SMA) was clamped. A vertical aortotomy was made. The defect of intima (5x2.5cm) was found at the anterior of the aorta. Celiac artery (CA) was cannulated and perfused by cardiopulmonary bypass blood. C, D: The bovine pericardial patch (7x3cm) angioplasty was performed with 3-0 Prolene continuous sutures using bovine pericardial strips with preserving intercostal arteries (Th10, 11,12). E: The aortotomy was closed using bovine pericardial strips.
Continuous cold perfusion of the kidneys was used in two patients (patients 1 and 2) with infected juxtarenal aortic aneurysm ( Figure 4). Mural thrombus was removed after aneurysm was incised, and then irrigated with saline solution. BPPs were used to close the defects with double 3-0 Prolene continuous sutures using bovine pericardial strips in seven patients. However, the arterial wall in 1 (patient 7) was too fragile to repair, resection of aneurysm and replacement with rifampicin-soaked Dacron graft was required ( Figure 6,7).

Figure 5.
Operative findings (patient 8). A: The aneurysm of the thoracoabdominal aorta was markedly expanded. Severe adhesion around the aneurysm was observed. CA and SMA were exposed and taped. B: A vertical aortotomy was made. The defect of intima (5x2.5cm) was found at the anterior of the aorta. C: The bovine pericardial patch (3x7cm) angioplasty was performed with 3-0 Prolene continuous sutures using bovine pericardial strips with preserving intercostal arteries (Th10, 11,12). D: The aortotomy was closed using bovine pericardial strips. In one patient (patient 5) had an aneurysm ruptured into colon preoperatively, a colostomy was performed simultaneously. Retroperitoneal spaces were implanted with greater omentum in six patients.
Written informed consent was achieved from all patients before the operation.

Results
There was no surgical/hospital death. The blood cultures demonstrated positive for α-streptococcus in one patient (patient 6) and seven patients negative. The intraoperative abscess cultures showed positive for methicillin-resistant Staphylococcus aureus (MRSA) in one patient (patient 5) and seven patients negative. There was no surgical/hospital death. There were two late deaths at follow-up. A 74-year-old man (patient 6) who had an infrarenal abdominal aortic aneurysm with aortosigmoid colon fistula with melena had a BPPA with omentopexy and colostomy. The patient was re-admitted to the hospital with vomiting blood four months after surgery, and he underwent a total gastric resection due to hemorrhagic gastric ulcer, but the patch angioplasty site became a re-mass, ruptured and died ( Figure 8). Another patient (patient 5) died at his home 12 months after surgery, and the cause of death was unknown (Figure 9).

Discussion
IAA is a life-threatening condition with difficult treatment and poor survival. In addition to systemic antibiotic treatment, complete removal of the infected aorta, debridement of the surrounding tissue, and in situ aortic reconstruction is the standard procedure for treating IAA, but which graft material is best is a matter of debate.
Although use of an autologous arterial patch for IAA has been reported [7], to our knowledge, there have been no cases except for the case who we have previously published [8] that underwent reconstructive surgery using BPPA. BPPA for infected thoracoabdominal aortic aneurysm in our patients (patients 4 and 8) has been challenging. A search of the literature retrieved no publications that described the same procedure for infected thoracoabdominal aortic aneurysm.
Garcia et al. [4] present five cases of vascular reconstruction using BPP for the field of infection in immunosuppressive transplant patients and state that the use of autologous grafts in these patients is likely to significantly increase operative time and give another site to the risk of infection, however BPP is quickly accessible and useful.
McMillan et al. [6] used BPPs to repair infected fields of 51 arteriotomies in 48 consecutive patient undergoing removal of infected polytetrafluoroethylene grafts, and 50 of the 51 patches remained in place over a mean follow-up period of 2.1 years without evidence of recurrent infection, rupture, or revision. They concluded that BPP provides a durable option to saphenous vein for arterial reconstruction following removal of infected arterial grafts.
Bovine pericardium does not require long-term anticoagulation and has been associated with a lower risk of infection and thrombosis compared to synthetic materials. The patch material most proved durable in the arterial applications as a patch for carotid endarterectomy [15]. There are several case reports of BPP used for cardiac and pulmonary reconstruction in infected fields, and they have indicated good results and durability [5,16]. The definitive low rate of infection linked to BPPs has suggested that BPPs may be resistant to infection and therefore might be an suitable material to use in the presence of infection [6]. There was the following as positive characteristics of this bioprosthetic material: the soft-ness of the biological tissue, which permits simple surgical handling, the good coaptation to suture lines resulting in a hemostatic anastomosis, and the lower thrombogenicity of glutaraldehyde-treated collagen tissue [17,18].
BPPA has low invasiveness because it minimizes the dissection range around the aneurysm, and handling of bovine pericardium is easy, which may shorten the operative time. In addition, bovine pericardium causes fewer cases of infection due to the antimicrobial effect of glutaraldehyde compared with those caused by a Dacron graft [19] which suggests that patch angioplasty using bovine pericardium is useful for treatment of saccular IAA that is hard to dissect. However, when the tissue is fragile and patch angioplasty is considered difficult, it is significant to remove the fragile tissue and infection focus immediately and accomplish in situ aortic replacement as in patient 7. False aneurysm formation long after patch angioplasty of saccular aortic aneurysm with an artificial graft has been reported [20], suggesting the necessity of careful follow-up.
There were two late deaths in the present series. In these cases where the aneurysm is adhered to the sigmoid colon with melena as in patients 5 and 6, reconstruction using bovine roll graft may be better than patch angioplasty because it seems to be more infectious [11,12].
Considering the characteristic feature of saccular form in IAA and to save the renal ischemic time, we performed a BPPA of the aneurysmal neck. We found that the renal ischemic time was acceptable with this procedure as in patient 1 and patient 2. A standardized strategy to routinely apply renal hypothermia during the ischemic period of elective juxtarenal aortic aneurysm surgery may reduce postoperative renal failure [21]. Endovascular aortic repair (EVAR) is a less invasive alternative to traditional open repair of IAA. A major disadvantage is that the infected tissue, including the aneurysm itself, is not removed, which may cause persistent sepsis and infection of endoprosthesis. EVAR could be considered a temporizing alternative or a bridge to later elective open repair [2,22].
Because long-term results of this procedure are still unknown, long-term antibiotic treatment was given postoperatively. Recently, PET/CT scan was applied in the diagnosis of infected aortic aneurysm. Reeps et al. [23] reported finding of increased aortic FDG uptake on FDG-PET/CT scan was correlated with inflammation, histopathologic characteristics of aneurysm wall instability, and clinical symptoms. Moreover, PET/CT made an important contribution for monitoring response to antibiotic treatment. The optimal duration of antibiotic cover is a matter for expert opinion, although prospective use of PET/CT to determine inflammatory activity could prove valuable to guide such recommendations [24].

Conclusion
Surgical outcome for IAA was satisfactory. BPPA could be one of the surgical options, especially in patients with severe adhesion around the aneurysm. The long-term follow-up is warranted to further validate the advantage/disadvantage.