Successful endovascular management of multiple mycotic aneurysms after liver transplantation – A case report and review of the literature

Abstract

Background

Mycotic vascular complications after liver transplantation are rare but can be pose a serious threat to the liver graft and the patient’s life. Mycotic complications can present as an incidental finding on routine imaging, or as haemorrhagic shock. Traditionally, these mycotic vascular complications were managed with open surgery.

Method/results

In this case report, we describe a patient who had developed multiple sequential mycotic aneurysms after liver transplantation which were managed successfully using endovascular and percutaneous techniques.

Conclusion

An endovascular approach is minimally invasive and will be the way forward in managing these mycotic vascular complications.

Keywords

Mycotic aneurysm endovascular liver transplantation

Case report

Our patient is a 57-year-old female of Chinese ethnicity who is diagnosed with cryptogenic liver cirrhosis which was complicated by portal hypertension, thrombocytopenia and oesophageal varices since 2009. She was evaluated for liver transplantation in March 2016 when her Model for End-Stage Liver Disease (MELD) score was 16. Pre-liver transplant evaluation was unremarkable.

First living-related donor liver transplant

The patient underwent a living-related donor liver transplant (LDLT) in June 2016 using a right lobe graft. Hepatic vein and portal vein anastomoses were unremarkable. The recipient gastroduodenal artery was used for anastomosis to the graft right hepatic artery for arterial in-flow as the anastomosis between the recipient right hepatic artery and graft right hepatic artery was unsuccessful. Although intra-operative ultrasound demonstrated good pulsatile flow, hepatic artery thrombosis occurred on post-operative day 4. Emergent catheter directed thrombolysis failed to re-establish hepatic artery flow and the patient was scheduled for a second LDLT.

Second living-related donor liver transplant

The patient underwent a second LDLT in July 2016 using a right lobe graft. Arterial in-flow was supplied via an arterial conduit from the infra-renal aorta comprising of a cadaveric iliac artery allograft and a radial artery autograft. Hepatic vein and portal vein anastomoses were unremarkable. After completion of the arterial anastomoses, good and pulsatile arterial flow was demonstrated on intra-operative ultrasound. Despite therapeutic anticoagulation, thrombosis of the arterial graft occurred on post-operative day 26. Attempts at revascularization were unsuccessful and the patient was placed on the deceased donor liver transplant waiting list. In the post-operative period, the patient developed Enterococcus faecium bacteraemia secondary to an infected biloma which was treated with percutaneous drainage and a prolonged course of intravenous Vancomycin.

Deceased donor liver transplant

The patient underwent a deceased donor liver transplant (DDLT) in September 2016 using a full liver graft. A cadaveric iliac artery allograft was anastomosed to the supra-coeliac aorta to facilitate the arterial anastomosis during warm ischaemia. Hepatic vein and portal vein anastomoses were unremarkable. Arterial in-flow to the graft was completed after the gastroduodenal artery from the deceased donor graft was anastomosed to the cadaveric iliac artery allograft. Post-operatively, arterial in-flow remained patent, but the patient developed Candida krusei fungaemia which was treated with an extended course of intravenous Anidulafungin.

Infra-renal mycotic aortic aneurysm

Computed tomography (CT) scan of the abdomen performed on post-operative day 56 (from DDLT) to evaluate for a cause of pyrexia demonstrated a 32 mm saccular outpouching from the infra-renal aorta at the base of the infra-renal aorta arterial conduit suggestive of a mycotic aneurysm (Figure 1(a)). An endovascular approach was deemed more appropriate for this patient in view of her elevated perioperative risks, as well as the difficulty to re-enter a hostile abdomen if an open repair was undertaken. Urgent endovascular aortic repair (EVAR) was performed, with placement a straight aortic endograft (Cook Medical, Bloomington, IN, USA) within the infra-renal aorta (Figure 1(b) and (c)). Although no positive blood cultures were obtained, the aetiology of the mycotic aneurysm was presumed to be due to Enterococcus faecium or Candida krusei. Follow-up CT angiography performed one week later revealed a possible type 1B endoleak, and a bifurcated aortic endograft (Cook Medical, Bloomington, IN, USA) was deployed within the existing stent graft to re-line and extend the seal zones with successful complete exclusion of the mycotic aneurysm, as demonstrated on completion aortogram and follow-up CT angiography.

Figure 1.

(a) Computed tomography scan demonstrating a saccular aneurysm arising from the infra-renal aorta. (b) Digital subtraction aortography demonstrating the infra-renal aneurysm. (c) Successful deployment of a straight aortic endograft across the infra-renal aneurysm.

Supra-coeliac mycotic hepatic artery pseudoaneurysms

CT angiography performed on post-operative day 107 (from DDLT) to evaluate for persistent pyrexia revealed the presence of two saccular pseudoaneurysms arising along the course of the supra-coeliac aorta arterial conduit (Figure 2(a) and (b)). EVAR was performed with initial chimney stenting of the supra-coeliac conduit with BeGraft (Bentley Innomed, Hechingen, Germany) and Viabahn (Gore Medical, Flagstaff, AZ, USA) covered stents to exclude both pseudoaneurysms, followed by placement of a straight aortic endograft (Cook Medical, Bloomington, IN, USA) above the coeliac axis (Figure 2(c) and (d)). Interval CT after chimney stenting and EVAR demonstrated complete thrombosis of the distal pseudoaneurysm and partial thrombosis of the proximal pseudoaneurysm. Percutaneous thrombin injection into the proximal pseudoaneurysm sac under ultrasound guidance was performed to attain complete thrombosis. Blood cultures obtained from a vascular sheath placed within the supra-coeliac aorta arterial conduit during chimney stenting and EVAR yielded Proteus mirabilis. The patient was planned to receive three months of intravenous Vancomycin, Anidulafungin and Ceftriaxone in consideration of all possible mycotic aetiologies, followed by lifelong suppressive oral levofloxacin. A follow-up CT angiography performed one month after showed complete exclusion of all mycotic aneurysms and pseudoaneurysms with no evidence of endoleak.

Figure 2.

(a) Computed tomography scan showing a pseudoaneurysm arising from the supracoeliac aorta arterial conduit. (b) Computed tomography scan showing a second pseudoaneurysm arising from the supracoeliac aorta arterial conduit. (c) Digital subtraction angiography demonstrating both pseudoaneurysms. (d) Successful chimney stenting of the supracoeliac aorta arterial conduit and deployment of a straight aortic endograft with total exclusion of the pseudoaneurysms.

Follow-up

Since discharge, the patient was placed on regular follow-up with the National University Centre for Organ Transplantation (NUCOT) clinic. She was last reviewed in March 2019 in which a repeat CT angiography revealed preserved hepatic artery opacification and a stable appearance of the patent aortic/iliac stent graft. In view of the patient’s propensity for developing thrombotic complications, a hypercoagulable work-up was pursued, which was negative.

Discussion

Mycotic aneurysms or pseudoaneurysms are rare vascular complications after liver transplantation. These mycotic vascular complications occur in less than 1% of patients after liver transplantation, and early diagnosis with prompt intervention is the key to preventing catastrophic sequelae such as massive intraperitoneal haemorrhage, hepatic artery thrombosis, graft loss and death.¹ Although mycotic vascular complications can occur anywhere in the body, they most commonly involve the aorta, arterial conduit or hepatic artery, where prior anastomoses or surgical reconstruction had been performed during liver transplantation. A summary of all reported cases of mycotic vascular complications after liver transplantation in current literature is provided in Table 1.

Table 1.

Mycotic vascular complications after liver transplantation in current literature.

Author	Clinical presentation	Case details	Isolated organism(s)	Risk factors	Treatment	Outcome
Fichelle et al.²	Sepsis	Coeliac artery dissection associated with mycotic hepatic artery pseudoaneurysm	Staphylococcus aureus	N.A.	Arterial reconstruction with autologous saphenous vein graft	Alive
Rudich et al.³	Haemobilia	Mycotic hepatic artery pseudoaneurysms with fistulation into the biliary tree	Aspergillus fumigatus, Enterococcus spp.	Re-operation for bile peritonitis	Arterial reconstruction with autologous saphenous vein graft	Alive
Goldman et al.⁴	Upper gastrointestinal haemorrhage	Mycotic aneurysm of infra-renal aortic conduit with aortoenteric fistula	N.A.	Use of aortic conduit (iliac artery allograft), re-transplant on post-operative day 9	N.A.	Death
Sheiner et al.⁵	Intra-abdominal haemorrhage	Mycotic infra-renal aorta and hepatic artery pseudoaneurysms	Candida spp., Enterococcus faecium	Re-operation for early hepatic artery thrombosis, use of infra-renal aortic conduit (iliac artery allograft)	Aortic replacement with a Goretex tube graft, PTFE extension anastomosed from tube graft to healthy segment of previous aortic conduit	Alive
Leonardi et al.⁶	Haemobilia	Mycotic hepatic artery pseudoaneurysms with fistulation into the biliary tree	N.A.	Post-operative bile leak treated with percutaneous drainage	Arterial reconstruction with autologous saphenous vein graft	Alive
Alamo et al.⁷	Haemobilia	Mycotic hepatic artery pseudoaneurysms with fistulation into the biliary tree	Pseudomonas spp., Enterobacterium spp.	N.A.	Explantation of transplanted liver due severe hepatic necrosis	Death
Jones et al.⁸	Intra-abdominal haemorrhage	Ruptured mycotic hepatic artery aneurysm	Methicillin resistant Staphylococcus aureus, Candida albicans	Re-operation for bile leak, re-transplant for hepatic artery thrombosis, use of aortic conduit	N.A.	Death
Jones et al.⁸	Elevated liver transaminases	Mycotic hepatic artery aneurysm	Methicillin resistant Staphylococcus aureus	Temporary abdominal closure and delayed abdominal closure	Endovascular coiling and subsequent surgical excision and ligation of hepatic artery aneurysm	Death
Camagni et al.⁹	Intra-abdominal haemorrhage	Ruptured mycotic hepatic artery aneurysm	Candida albicans	N.A.	Primary repair of hepatic artery	Death
	Intra-abdominal haemorrhage	Ruptured mycotic hepatic artery aneurysm	Enterococcus spp., Staphylococcus coag. neg., Proteus mirabilis, Candida albicans	Infected full layer dehiscence of surgical wound requiring surgical revision	Hepatic artery partial resection and re-anastomosis	Death
	Intra-abdominal haemorrhage	Ruptured mycotic hepatic artery aneurysm	Candida albicans, Pseudomonas aeruginosa	Biliary leak requiring percutaneous drainage and internal-external biliary stent	Occlusion of hepatic artery inflow with subsequent re-transplantation	Alive
	Intra-abdominal haemorrhage	Ruptured mycotic hepatic artery aneurysm	Candida albicans, Enterobacter cloacae, Pseudomonas aeruginosa, Enterococcus faecium, Aeromonas spp.	Hyperacute rejection requiring hyper-immunosuppressive protocol	Primary repair of hepatic artery complicated by liver ischemia requiring liver explantation with portocaval anastomosis	Death

Mycotic vascular complications can be asymptomatic and diagnosed incidentally on imaging or can manifest with subtle presentations such as pyrexia or deranged liver transaminases.⁸ However, most mycotic vascular complications are diagnosed when patients present with clinically established syndromes as haemorrhagic shock. Mycotic pseudoaneurysms involving the hepatic artery can present with sepsis due to recurrent bacteraemia, or haemobilia secondary to fistulation into the biliary tree.^2,3,6,7 Similarly, mycotic aneurysms of the aorta or arterial conduits can present with massive upper gastrointestinal bleeding due to an aortoenteric fistula.⁴ The eventual end-point of a mycotic aneurysm or pseudoaneurysm inevitably ends with rupture, and patients can present with sudden intraperitoneal haemorrhage due to rupture.^5,8,9

The diagnosis of a mycotic vascular complication is made when a positive blood culture is present, or if organisms are isolated from the aneurysmal tissue obtained during surgery. Staphylococcus aureus and Salmonella are the most common organisms associated with the development of mycotic aneurysms due to their propensity to adhere to arterial walls.¹⁰ However, as patients after liver transplantation receive immunosuppression, organisms which are typically not associated with mycotic aneurysms such as Enterococcus spp., Candida spp., and Aspergillus fumigatus are equally as common and have been described in literature.³^,^5,8 Moreover, like our reported patient, mycotic vascular complications after liver transplantation tended to be associated with multiple organisms.

Several risk factors such as the use of arterial conduits with multiple vascular anastomoses, perioperative systemic or intra-abdominal infection, bile leaks, re-laparotomy and re-transplantation have been postulated to increase the risk of development of mycotic complications after liver transplantation.^3–6,8 These factors increase the risk of mycotic complications by causing direct bacterial inoculation during the time of surgery, bacteraemic seeding or direct extension of a local infection.

Although the gold standard investigation for the imaging diagnosis of a mycotic aneurysm or pseudoaneurysm is conventional angiography, non-invasive imaging options such as conventional Doppler ultrasound, contrast enhanced ultrasound, magnetic resonance angiography or CT angiography can be utilized. If suspecting a mycotic vascular complication after liver transplantation, CT angiography is the most useful due to its ability to accurately demonstrate the aneurysm or pseudoaneurysm with its associated vasculature and adjacent viscus. CT findings of perianeurysmal inflammation, oedema, soft tissue mass or gas locules may suggest a mycotic aetiology.¹¹

Traditionally, mycotic aneurysms or pseudoaneurysms are treated with surgical debridement of the infected vessel, with or without revascularization to restore blood flow depending on the vessel involved. Management of mycotic hepatic artery aneurysms or pseudoaneurysms can be challenging due to the need to preserve or restore arterial in-flow to the transplanted liver. In the past, some authors have treated hepatic artery pseudoaneurysms with simple ligation, but complications such as graft necrosis or biliary strictures have led to its abandonment.¹² Restoring arterial in-flow to the liver is mandatory, and several authors have reported successful management with excision of the mycotic hepatic artery and arterial reconstruction with an autologous saphenous vein graft originating from an uninfected field.^2,3^,⁶ Mycotic aneurysms involving the aorta may develop after the use of an arterial conduit and can be managed with open aortic replacement with a synthetic tube graft.⁵

Alternatively, in recent years, endovascular techniques have been utilized in the management of mycotic aneurysms or pseudoaneurysms, especially in patients with a prohibitive risk of open surgery. In our report, we described a patient who developed sequential mycotic vascular complications which were treated using endovascular stenting. To our knowledge, this is the first report of successful endovascular treatment of mycotic complications in a liver transplant patient, although one author has described the use of endovascular coiling as a bridge to open surgery in the management of a mycotic hepatic artery aneurysm.⁸ The minimally invasive nature of endovascular treatment renders it an attractive management option, although long-term durability is uncertain. These patients will also require lifelong suppressive antibiotics and regular follow-up.¹³

Footnotes

Authors’ note

Informed consent has been sought from the patient for this case report.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Tan Jarrod Kah Hwee

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