Superficial temporal artery-middle cerebral artery bypass for progressive cerebral infarction in invasive aspergillosis-induced total occlusion of internal carotid artery: A rare case and literature review

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Korean J Cerebrovasc Surg. 2025;.jcen.2025.E2024.06.003

Publication date (electronic) : 2025 April 8

doi : https://doi.org/10.7461/jcen.2025.E2024.06.003

Minje Jeon¹, Sung-Tae Kim^,2, Suckyoon Lee³, Jin Lee¹, Jung Hae Ko⁴, Se-Young Pyo¹, Won-Hee Lee¹, Hangwoo Lee⁵, Yeong Gyun Jeong¹

¹Department of Neurosurgery, Busan Paik Hospital, Inje University, School of Medicine, Busan, Korea

²Department of Neurosurgery, Haeundae Paik Hospital, Inje University, School of Medicine, Busan, Korea

³Department of Neurology, Busan Paik Hospital, Inje University, School of Medicine, Busan, Korea

⁴Department of Internal medicine, Haeundae Paik Hospital, Inje University, School of Medicine, Busan, Korea

⁵Department of Neurosurgery, Busan St. Mary’s Hospital, Busan, Korea

Correspondence to Sung-Tae Kim Department of Neurosurgery, Haeundae Paik Hospital, Inje University, School of Medicine, 875, Haeun-daero, Haeundae-gu, Busan, 48108, Korea Tel +82-51-890-6144 E-mail kimst015@hanmail.net

Received 2024 June 6; Revised 2025 March 12; Accepted 2025 March 22.

Abstract

INTRODUCTION

Aspergillosis is an opportunistic infection often affecting immunosuppressed individuals, including, those with haematologic malignancies, uncontrolled diabetes, neutropenia, human immunodeficiency virus, acquired immunodeficiency syndrome, or those undergoing transplant procedures [1,3,23]. This infection can invade the central nervous system (CNS) through hematogenous dissemination from the respiratory system, leading to abscesses, fungal balls, and meningitis [22,24]. Alternatively, Aspergillus sinusitis may extend from the skull base to the brain’s vascular system to bring about the same complications [15,29,30,35]. CNS involvement represents the most severe form of invasive aspergillosis, with mortality rates exceeding 90% [1,3,19,23,34]. Such cases may cause vasculitis in cerebral arteries, leading to the development of thromboses, septic emboli, cerebral infarction, mycotic aneurysms, and subarachnoid haemorrhages (SAHs), all of which significantly impact mortality [5,10,21].

Several surgical interventions for CNS aspergillosis have primarily focused on endovascular approaches [30]. Open surgeries, such as artery ligation, endarterectomy, and high-flow bypass for mycotic aneurysms, are uncommon and often result in high mortality rates [11,29,30,35]. There have been no reported cases of using the superficial temporal artery to middle cerebral artery (STA-MCA) bypass for total cerebral artery occlusion resulting from CNS aspergillosis. This may be due to difficulties in diagnosing the condition and rapid progression of the disease [9,19,27].

This case report details a successful STA-MCA bypass in a patient with ischaemic stroke due to CNS aspergillosis-induced internal carotid artery (ICA) occlusion.

CASE DESCRIPTION

The study protocol was reviewed and approved by the relevant Institutional Review Board, ensuring compliance with all relevant regulations.

A 59-year-old male presented to the ophthalmology outpatient clinic with a 3-day history of right eye ptosis. Intranasal examination revealed mucosal injection, bleeding, and whitish patches. Although cranial magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) demonstrated patent blood flow, they also showed extended sinusitis with periocular inflammation, prompting immediate admission (Fig. 1A and 1B).

Fig. 1.

Contrast-enhanced brain magnetic resonance imaging (MRI) and time-of-flight (TOF) angiography performed on hospital day 1 (3 days from initial symptom onset). (A) There is evidence of periocular soft tissue infection and neuritis (White arrow). (B) Magnetic Resonance Angiography (MRA) reveals non-specific findings, except for a focal vascular bulge in the contour of the right A1 segment.

Upon admission, slightly elevated C-reactive protein (CRP) (5.77 mg/L) and erythrocyte sedimentation rate (ESR) (45 mm/h) levels were observed. Although the patient denied a history of diabetes mellitus, an HbA1c level of 12.8% was found, indicating poorly controlled diabetes mellitus. Endoscopic biopsy of the paranasal sinus was performed, and intravenous antibiotic (ceftriaxone and metronidazole) and antifungal (amphotericin B) therapies were initiated.

Eight days after symptom onset (hospital day [HD] 6), the patient developed complete vision loss in the right eye and sudden left-sided hemiplegia and neglect (National Institutes of Health Stroke Scale [NIHSS] score: 10). Perfusion computed tomography (CT) and CT angiography confirmed acute cerebral infarction (Fig. 2A and 2B), which resulted in hemiparesis leading to head trauma. A history of head trauma is a contraindicator for intravenous tissue plasminogen activator (TPA); thus, endovascular treatment was attempted. Conventional angiography revealed severe stenosis with luminal irregularities in the right distal ICA, suggestive of vasculitis. Given these findings, mechanical thrombectomy was deferred. To address potential platelet aggregation, 1 mg of intra-arterial Aggrastat (tirofiban hydrochloride, Aggrastat, Medicure, United States) was administered, followed by a 24-hour infusion of intravenous Aggrastat. Post-procedural diffusion MRI was performed afterwards (Fig. 2C and 2D). Following intra-arterial thrombolysis, oral antiplatelets (aspirin and clopidogrel) were administered; thereafter, his neurological symptoms stabilised.

Fig. 2.

Initial radiologic findings following cerebral infarction due to central nervous system (CNS) aspergillosis-induced right internal carotid artery (ICA) occlusion. (A) Time-to-maximum (Tmax >6 seconds) prolongation suggests cerebral infarction in the right hemisphere. (B) Computed tomography (CT) angiography shows a white arrow highlighting the distal ICA stenosis and contrast enhancement defect at the proximal M1 segment. (C) The dashed arrow in the anteroposterior view of cerebral angiography indicates invasive aspergillosis-associated septic thrombi at the ICA bifurcation. (D) Post-intra-arterial thrombolysis diffusion magnetic resonance imaging (MRI) scan indicates ischemic changes in the watershed zone of the right middle cerebral artery.

Intranasal biopsy and right eye enucleation confirmed invasive aspergillosis, indicating antifungal therapy as the mainstay of treatment. On HD 35, the patient demonstrated mild left-sided hemiparesis (NIHSS score: 3) and was discharged with a regimen of oral aspirin, voriconazole, metronidazole, and cefpodoxime.

Approximately 3 months later (110 days from initial onset), the patient developed relapse of left-sided hemiparesis. He underwent MRI and cerebral angiography, revealing multifocal infarctions in the right cerebral border zone and severe right ICA stenosis (Fig. 3A and 3B). History taking on readmission revealed a 5-week history of medication non-adherence. Physical and diagnostic examinations confirmed left-sided hemiparesis (NIHSS score: 7), exacerbated sinusitis, and elevated CRP levels (6.47 mg/L). Perfusion MRI further showed delayed cerebral perfusion, and vessel wall MRI was suggestive of chronic perivascular inflammation and stenosis (Fig. 3C and 3D). A dual antiplatelet (aspirin and clopidogrel) and antifungal (voriconazole) regimen was initiated for treatment.

Fig. 3.

Radiologic findings during the second cerebral event in aspergillosis-induced right internal carotid artery (ICA) stenosis. (A) Diffusion magnetic resonance imaging (MRI) reveals multifocal lacunar infarctions. (B) Right common carotid angiography (lateral view) shows severe stenosis in the posterior genu of the ICA cavernous segment and ICA bifurcation (black arrows), with compromised antegrade blood flow. The superficial temporal artery appears well-developed (black dashed arrow). (C) Magnetic resonance (MR) perfusion imaging time-to-peak sequences indicate cerebral hypoperfusion in territories of the right middle cerebral artery and both anterior cerebral arteries. (D) Hyperintensity along the ICA bifurcation wall (arrow) suggests vasculitis in the lesion.

On HD 3, the patient developed worsening left-sided weakness (NIHSS score: 9), and MRI revealed progressive ischaemic damage in the right cerebral border zone. Induced hypertension (systolic blood pressure >180 mmHg) was initiated for symptom management, and voriconazole was shifted to IV amphotericin B. Despite these changes, the patient’s condition progressively deteriorated, with new-onset severe left-arm weakness (motor grade: 1/5, NIHSS score: 10). Subsequent MRI scans revealed additional ischaemic lesions (Fig. 4A).

Fig. 4.

Further progression of ischemic lesions in the right hemisphere border-zone. (A) On diffusion magnetic resonance imaging (MRI), further progression is detected. (B) Microscopic view of the superficial temporal artery (STA)-middle cerebral artery (MCA) anastomosis site before the temporary clips are removed. STA-MCA bypass surgery is conducted on hospital day 12 (121 days from initial onset). (C) Intraoperative indocyanine green (ICG) angiography confirms the patency of the bypass graft.

The patient received a 10-day course of induced hypertension therapy, with minimal improvement in motor function. During this time, new cognitive deficits in memory and language were observed. By HD 12 (121 days from initial onset), the patient exhibited complete paralysis of the left arm (NIHSS score: 11), prompting us to perform an STA-MCA bypass (Fig. 4B and 4C). This microsurgical procedure involved an end-to-side anastomosis of the parietal branch of the STA to the M4 segment of the MCA using 10-0 nylon sutures. Intraoperative imaging confirmed successful revascularisation.

While the patient reported persistence of left-sided hemiparesis (NIHSS score: 11), cognitive function improved postoperatively, allowing for the discontinuation of induced hypertension therapy. CT angiography confirmed a patent bypass graft, and there was noticeable improvement in blood flow at the bypass site (Fig. 5A). A second sinus debridement was performed within a few days postoperatively. On HD 40, the patient was discharged after demonstrating improvement in neurological symptoms (left arm motor grade: 1/5, left leg motor grade: 3/5, NIHSS score: 10). During follow-ups in our outpatient clinic, his motor skills gradually improved over time (left arm motor grade: 2/5, left leg motor grade: 3/5, NIHSS score: 8, modified Rankin Scale score: 4). CT angiography and perfusion image at 4 months post-operation confirmed the patency of the bypass graft (Fig. 5B, 5C and 5D). This suggests that the additional STA flow played a crucial role in preventing the progression of the infarction. Antifungal therapy was discontinued 16 months postoperatively, as enhanced MR imaging showed well-controlled aspergillosis (Fig. 6A and 6B). Additionally, the 16-month MRA demonstrates well-preserved blood flow from the STA to the MCA, with the patient’s neurological recovery remaining gradual yet stable over nearly two years (Fig. 6C).

Fig. 5.

Postoperative imaging. (A) Perfusion computed tomography (CT) performed 5 days postoperatively shows improved time-to-maximum (Tmax) values in the area supplied by the bypassed vessel. However, Tmax delays persist in the territories of the right middle cerebral artery and both anterior cerebral arteries. (B) CT angiography at 4 months post-operation demonstrates patent blood flow through the bypass graft. (C, D) Perfusion CT at 4 months post-operation shows that although the reversed blood supply from the superficial temporal artery (STA) is inherently limited in the Tmax image, the bypass site demonstrates improvement. This implies that a stable cerebral blood flow has been maintained in conjunction with the bypassed vessel.

Fig. 6.

Postoperative imaging at 16 months. (A, B) In the T1-enhanced magnetic resonance (MR) imaging, the degree of contrast enhancement near the right cavernous sinus significantly decreased, leading to the discontinuation of antifungal therapy following imaging evaluation. (C) Due to the inherent limitations of time-of-flight (TOF) angiography in visualizing small vessels with low blood flow, some of the smaller vessels observed in the previous follow-up computed tomography angiography (CTA) are not visible. However, the preserved blood flow from the superficial temporal artery (STA) to the middle cerebral artery (MCA) is clearly demonstrated (red circle).

DISCUSSION

CNS aspergillosis, characterised by its rapid progression and high mortality rates, often leads to cerebral artery occlusions or mycotic aneurysms that are typically confirmed postmortem [1,10,13,26,34]. Since pathological confirmation is ideal for definitive diagnosis, difficulties in early detection result in frequent treatment failure [19,33]. Moreover, alternative diagnostic tools, including serum galactomannan, cerebrospinal fluid, and bronchoalveolar lavage, have limitations. In this case, repeated serum galactomannan tests yielded negative results [4,7,9,17,25], and polymerase chain reaction was not utilised as a potential diagnostic tool [19].

The standard treatment for invasive aspergillosis includes surgical debridement combined with antifungal medications, such as voriconazole and amphotericin B [4,9,23,28,30]. For CNS aspergillosis, IV steroids may be considered despite their potential risk of worsening infections [4,29]. Surgical interventions for CNS aspergillosis are rarely performed, with few case studies that were managed with bypass surgery [11,29,30,35].

One study by Takemoto et al. [30] reported the successful treatment of an 82-year-old female with a large mycotic aneurysm due to contralateral maxillary aspergillosis sinusitis using endovascular ligation of the right ICA with antifungal and antiplatelet therapies. Another study by Shinya et al. [29] described the performance of trapping surgeries for dual mycotic aneurysms in a 77-year-old male with successive SAHs. Despite the surgical interventions in this case, the patient succumbed to medication-induced renal failure. Yamaguchi et al. [35] reported a successful high-flow bypass procedure combined with trapping of the right ICA mycotic aneurysm in a 79-year-old male who survived with antifungal treatment.

Lastly, Lange et al. [11] analysed the 10-year treatment outcomes of 10 patients with CNS aspergillosis, reporting a 60% mortality rate, which was significantly lower than that in previous reports. Although, it should be noted that majority of their surgeries involved abscess drainage or evacuation. Among their few vascular interventions, one patient underwent bypass surgery for a mycotic anterior communicating artery aneurysm, and another underwent thromboendarterectomy for a thrombosed ICA with septic emboli; both had fatal outcomes [11].

Cerebral infarction typically results from atherosclerosis, but sometimes it can be from endothelial damage, embolism, trauma, and inflammatory conditions [2,14,20]. Due to the potential for collateral circulation formation, cerebral infarctions caused by atherosclerosis may have milder symptoms and slower progression compared to those caused by embolism. In this case, aspergillosis led to inflammatory occlusion in the right distal ICA, resulting in early-stage septic thromboembolism. The patient exhibited both the rapid onset typical of embolic infarction and the gradual worsening seen in atherosclerosis-induced infarction. The patient’s course benefited from early diagnosis and treatment; however, his condition relapsed, probably due to medication non-adherence. Interestingly, while initial angiography revealed right distal ICA stenosis, the patient’s mild symptoms suggest the development of collateral circulation, implying a possibly slow disease progression.

During the second cerebral infarction event, the right ICA was nearly occluded, limiting treatment options due to underlying inflammatory nature of invasive aspergillosis. The resulting hypoperfusion affected the territories of the right MCA and both anterior cerebral arteries, which are primarily supplied by the right A1 segment. Despite initial treatments, the patient’s neurological state continued to deteriorate, necessitating STA-MCA bypass surgery 12 days later.

Postoperatively, the patient’s hemodynamics improved significantly, allowing discontinuation of induced hypertension and facilitating stable recovery. Four months later, imaging revealed an enlarged bypass vessel and enhanced brain perfusion. The patient continued antifungal therapy for 1 year on outpatient basis. Even after the discontinuation of treatment, the patient remained stable on follow-ups.

While researchers continue to investigate the potential benefits of bypass surgery in cerebral infarction, its efficacy in such cases remains an ongoing debate [6,8,12,16,18,31,32]. Our report contributes to this discussion by providing valuable insights on the role of bypass surgery in gradually progressive large-vessel occlusion due to fungal infection. Furthermore, the study highlights the importance of determining the optimal timing for surgical intervention. Early bypass surgery prior to severe motor deficits could have led to significantly better outcomes in this patient.

Although interventional approaches are generally favoured over surgical approaches for severe vessel complications of CNS aspergillosis [30], surgery may be a viable option for select patients especially in whom endovascular thrombectomy is deemed risky due to severe vascular fragility from vasculitis, and for whom intra-arterial thrombolysis has proven ineffective. To the best of our knowledge, there have been no case reports on STA-MCA bypass surgery for total ICA occlusion due to aspergillosis-induced vasculitis. Our case’s favourable treatment outcome aligns with previous studies suggesting that bypass surgery is safe and effective in preventing and stabilizing neurological deterioration not only in the acute phase but also in the subacute and recurrent stages of cerebral hypoperfusion due to main trunk artery occlusion [36]. With antifungal therapy and supportive care in the outpatient clinic, the patient maintained stable neurologic function for over 22 months in this case. This report underscores the potential of STA-MCA bypass to prevent or improve neurological deterioration, implying its potential utility for CNS aspergillosis.

CONCLUSIONS

We present a rare case of cerebral infarction secondary to right ICA vasculitis in a patient with aspergillosis sinusitis. The patient achieved a stable neurological course following successful STA-MCA bypass, with a relatively long-term follow-up of 22 months, underscoring surgery as a viable alternative for refractory cases.

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