CC BY-NC-ND 4.0 · Asian J Neurosurg 2022; 17(04): 638-641
DOI: 10.1055/s-0042-1757629
Case Report

Direct Carotid-Cavernous Fistula Caused by Internal Carotid Artery Perforation by a Microcatheter Body during Mechanical Thrombectomy

Satoshi Miyamoto
1   Department of Neurosurgery, Mito Medical Center, Mito, Ibaraki, Japan
2   Division of Stroke Prevention and Treatment, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, Japan
3   Department of Neurosurgery, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, Japan
,
Noriyuki Kato
1   Department of Neurosurgery, Mito Medical Center, Mito, Ibaraki, Japan
,
Tomosato Yamazaki
1   Department of Neurosurgery, Mito Medical Center, Mito, Ibaraki, Japan
,
Akinari Yamano
1   Department of Neurosurgery, Mito Medical Center, Mito, Ibaraki, Japan
,
Yoshimitsu Akutsu
1   Department of Neurosurgery, Mito Medical Center, Mito, Ibaraki, Japan
,
Susumu Yasuda
1   Department of Neurosurgery, Mito Medical Center, Mito, Ibaraki, Japan
,
Yuji Matsumaru
2   Division of Stroke Prevention and Treatment, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, Japan
3   Department of Neurosurgery, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, Japan
,
Eiichi Ishikawa
3   Department of Neurosurgery, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, Japan
› Author Affiliations
 

Abstract

Rapid advances in emergent mechanical thrombectomy have resulted in a higher occurrence of arterial perforations during neurointerventions. Here, we report a case of internal carotid artery (ICA) perforation during mechanical thrombectomy in a 78-year-old man with a left middle cerebral artery occlusion. The ICA was perforated by a microcatheter during thrombectomy, forming a direct carotid-cavernous fistula. A two-stage drainer occlusion was conducted because of cortical venous reflex aggravation and ocular symptoms. Here, we report the perforation details and treatment, adding to evidence that ICA perforation with the microcatheter body is a concern during mechanical thrombectomy.


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Introduction

Recently, reports of internal carotid artery (ICA) perforation during neurointerventions, especially mechanical thrombectomy, have increased.[1] [2] [3] [4] Urgent procedures are typically performed via thrombectomy as early intervention and reperfusion strongly correlate with good prognoses[5]; however, this might be causative for the increased number of reported ICA perforations. Here, we report a rare case of an ICA perforation by the microcatheter body during mechanical thrombectomy that led to iatrogenic carotid-cavernous fistula (CCF) formation and then discuss treatment options for iatrogenic CCF during mechanical thrombectomy based on our outcome.


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Case History

A 76-year-old man with bloody stools was admitted to our hospital for a colonoscopy. His past medical history included atrial fibrillation, aortic valve stenosis, mitral valve regurgitation, hypertension, dyslipidemia, diabetes mellitus, and ascending colon cancer. He was taking apixaban for cardioembolic stroke prevention, which had been stopped for the colonoscopy. Two days after the colonoscopy, right hemiparesis, aphasia, and partial deviation of the eyes to the left occurred. The National Institute of Health Stroke Scale score was 23 and magnetic resonance imaging showed a left middle cerebral artery (MCA) occlusion requiring mechanical thrombectomy.

Mechanical Thrombectomy

A 9 F 25 cm sheath was placed in the right femoral artery and a 9F OPTIMO (Tokai Medical Products, Aichi, Japan) guide catheter was introduced to the cervical portion of the left ICA. Left internal carotid arteriography (ICAG) showed proximal M2 occlusion. While the Marksman microcatheter (Medtronic, Minneapolis, Minnesota, United States) was navigating to M2 over a Chikai 14 microwire (ASAHI Intecc, Aichi, Japan), strong pressure was needed to pass through the occlusion site. Suddenly, the loop shape of the microcatheter in the syphon portion changed significantly ([Fig. 1]). Left ICAG revealed a new direct CCF formation. Right ICAG showed cross-flow through the anterior communicating artery, supplying parts of the left MCA region, even though the M2 occlusion remained. The intervention was discontinued as we anticipated that left carotid compression twice a day would spontaneously close the CCF.

Zoom Image
Fig. 1 Mechanical thrombectomy: (A, B) Left ICAG revealing a left M2 proximal occlusion. (C) The microcatheter was advanced over a micro-guidewire. (D, arrow) The shape of the microcatheter changed significantly in the syphon portion of the ICA. (E, arrow) The body of the microcatheter perforated the ICA wall and went into the cavernous sinus. (F, G) Left ICAG revealed a direct CCF. Shunt flow was abundant and ascending blood flow to the brain diminished. This complication halted the thrombectomy.

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Carotid-Cavernous Fistula

However, proptosis, chemosis, and left extraocular movement dysfunction appeared on postoperative day 2 and treatment for symptomatic CCF was needed. Transvenous embolization failed because of the difficulty of the cavernous sinus (CS) approach; we then tried the transarterial approach and left ICAG showed a fistula at the medial posterior side of the ICA cavernous portion. The microcatheter was placed easily in the CS through the fistula, suspected to be quite large, and a high possibility of coil migration into the ICA was likely. Therefore, we only occluded dangerous drainers, such as the left infraorbital vein, the superior orbital vein, the superficial middle cerebral vein, the superior petrosal sinus, and the inter-CS, to decrease the shunt flow ([Fig. 2]). After the operation, left ocular symptoms improved. Carotid compression was maintained daily to induce clot formation within the direct CCF but right chemosis and proptosis appeared 3 months after the operation.

Zoom Image
Fig. 2 The first direct CCF treatment: (A, B) ICAG before the treatment: a fistula is visible in the posterior part of the ICA cavernous segment. Dangerous draining veins, including the left SOV, SMCV, SPS, and inter-CS, were occluded. (C, D) ICAG after treatment: shunt flow reduction was achieved and distal flow is visible.

The second intervention was planned as a parental artery occlusion because of the large fistula size. Left ICAG showed that the shunt flow drained mainly through a thin and clearly revealed inter-CS into the contralateral side of the CS. We thus switched to conduct sinus packing and occluded the inter-CS and left inferior petrosal sinus with a coil. Shunt flow diminished while anterograde flow was seen in the remaining small hollow of the CS ([Fig. 3]). Right ocular symptoms disappeared after the operation and the patient was transferred to another hospital with a modified Ranking Scale score of 5.

Zoom Image
Fig. 3 The second direct CCF treatment: (A, B) ICAG before the treatment: a thin inter-CS is clearly seen. We occluded the inter-CS and left inferior petrosal sinus with a coil. (C, D) ICAG after treatment: the direct CCF is diminished with only a small hollow at the fistula. Ascending flow to the brain was recovered.

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Discussion

Direct CCF

CCF is an abnormal connection between arteries and veins of the CS,[6] causing ocular symptoms such as proptosis, chemosis, ocular bruit, and increased intraocular pressure, which lead to ophthalmic nerve injury and possibly severe conditions like cranial nerve palsy or cerebral infarction.[3] [6] Head trauma, ruptured aneurysm, and idiopathic CCF are the main causes of direct CCF,[6] but some are iatrogenic in nature.[3] [6] [7] Recently, reports of ICA perforation and iatrogenic CCF in neurointervention have increased because of escalating usage of the inner catheter, more and more emergent treatment, and adaptation to the elderly with often torturous or stenotic vessels.[1] [2] [8] Although most iatrogenic CCF cases are type A by Barrow classification and their symptoms usually worsen rapidly,[1] [2] the ideal treatment time is still controversial.[9] Risk factors of iatrogenic CCF are usage of distal access catheters, female sex, and paraclinoid aneurysms.[8]


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Iatrogenic CCF Due to Mechanical Thrombectomy

Iatrogenic CCF occurrence is approximately 0.8% in interventional radiology, such as coil embolization of aneurysms and intracranial percutaneous transluminal angioplasty, but mechanical thrombectomy is only rarely causative.[8] We searched PubMed with the term “thrombectomy” and/or “iatrogenic CCF” and found only nine direct CCF cases during mechanical thrombectomy[1] [2] [3] [10] [11] [12] ([Table 1]); most of these (7 in 9) cases occurred during the stent-retriever procedure as this straightens the ICA and risks pull-out injury of small vessels such as the meningohypophyseal trunk. Of the reported cases, four in nine cases were symptomatic, all treated with interventional radiology, while five in six treated cases, including asymptomatic cases, were without recurrence after treatment.

Table 1

Summary of Iatrogenic direct CCFs occurring during mechanical thrombectomy

Study (yr)

Age/sex

Occlusion site

Procedure

CCF Sx

Treatment for CCF

Follow-up

Akpinar et al (2014)11

NA

Rt. distal ICA

Stent retriever and local aspiration

NA

Conservative

Died in a few days

Alan et al (2017)12

47

M

Rt. ICA terminus and MCA

Stent retriever and local aspiration

Conservative

Asymptomatic for 1.5 years

Alan et al (2017)12

NA

Lt. ICA terminus to M1

Stent retriever and local aspiration

Conservative

Asymptomatic for 4 months

Alan et al (2017)12

64

M

Rt. ICA and MCA

Stent retriever

+

Fistula occlusion

Asymptomatic for 2.5 years

Matsumoto et al (2018)1

67

F

Rt. M1

Stent retriever

+

Fistula occlusion

Asymptomatic for 3 months

Kurashiki et al (2019)2

87

F

Rt. M1

Stent retriever

+

Fistula occlusion

NA

Sheinberg et al (2020)3

78

F

Lt. MCA

Stent retriever and local aspiration

Fistula occlusion and pipeline

Asymptomatic for 6 months

Tsuji et al (2020)10

88

F

Lt. ICA cavernous portion

Micro guide wire navigation

Balloon catheter to occlude ICA

Asymptomatic

Current study

76

M

Lt. M2

Microcatheter navigation

+

Drainer occlusion

Asymptomatic

Abbreviations: +, symptomatic; –, asymptomatic; CCF, carotid-cavernous fistula; ICA, internal carotid artery; Lt., left; MCA, middle cerebral artery; NA, not available; Rt., right, Sx, symptom.


On the other hand, our case is the first case of direct CCF due to perforation with the microcatheter body. Regardless of cause, good reported outcomes of iatrogenic CCF during mechanical thrombectomy support interventional treatment.


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ICA Damage during Microcatheter Navigation

In our case, pushing the microcatheter through hard clots led to a bent microcatheter in the ICA cavernous portion and perforation with the microcatheter body. Kurashiki et al and Matsumoto et al reported that a linearized ICA during stent retrieval leads to small branch pull-out injuries and direct CCF, especially in patients with severe atheromatous arteries,[1] [2] and, as we experienced, microcatheter bending in torturous arteries can also cause ICA injury.

As CCF due to microcatheter body compression is presumed to have a larger fistula than guidewire tip, microcatheter tip, or pull-out injuries of the meningohypophyseal trunk, simple fistula occlusion is difficult and second-line treatments, such as a flow-diverting stent, sinus packing, or parental artery occlusion, are necessary.

Reports of ICA injury due to microcatheter body compression during neurointervention radiology are currently scarce but case numbers are expected to rise because of the steep increase in neurointervention for elderly people with severe atheromatous arteries.


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Conclusion

We experienced an iatrogenic CCF case due to ICA perforation with a microcatheter body during mechanical thrombectomy. We then conducted two-staged sinus packing and CCF occlusion was achieved. During mechanical thrombectomy, direct CCF formation during not only stent withdrawal but also microcatheter navigation is a constant concern.


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Conflict of Interest

Y.M. discloses lecturer fees from Medtronic, Stryker, Terumo, Johnson & Johnson?Cerenovas, Kaneka, Jimuro, and Medicos Hirata.

Acknowledgments

The authors would like to thank Dr. Alexander Zaboronok of the University of Tsukuba Faculty of Medicine Department of Neurosurgery for professional and language revision, and Dr. Bryan J. Mathis of the University of Tsukuba Hospital International Medical Center for language revision.

Informed Consent

The authors certify that they have obtained all appropriate patient consent.


  • References

  • 1 Matsumoto H, Nishiyama H, Takemoto H, Tetsuo Y, Nakao N. Carotid-cavernous fistula caused by vessel injury while withdrawing a stent retriever during mechanical thrombectomy for acute ischemic stroke: a case report. J Neuroendovasc Therapy 2018; 12 (05) 235-240
  • 2 Kurashiki Y, Hanaoka M, Sato K. et al. Occurrence of direct carotid-cavernous fistula during mechanical thrombectomy for middle cerebral artery occlusion. Tokushima Red Cross Hosp Med J 2019; 24: 82-89
  • 3 Sheinberg DL, Brunet MC, Chen SH, Luther E, Starke RM. Iatrogenic direct carotid-cavernous fistula following mechanical thrombectomy: a case report and review of the literature. Cureus 2020; 12 (04) e7524
  • 4 Ryu CW, Lee CY, Koh JS, Choi SK, Kim EJ. Vascular perforation during coil embolization of an intracranial aneurysm: the incidence, mechanism, and clinical outcome. Neurointervention 2011; 6 (01) 17-22
  • 5 Bourcier R, Goyal M, Liebeskind DS. et al; HERMES Trialists Collaboration. Association of time from stroke onset to groin puncture with quality of reperfusion after mechanical thrombectomy: a meta-analysis of individual patient data from 7 randomized clinical trials. JAMA Neurol 2019; 76 (04) 405-411
  • 6 Henderson AD, Miller NR. Carotid-cavernous fistula: current concepts in aetiology, investigation, and management. Eye (Lond) 2018; 32 (02) 164-172
  • 7 Lewis AI, Tomsick TA, Tew Jr JM. Management of 100 consecutive direct carotid-cavernous fistulas: results of treatment with detachable balloons. Neurosurgery 1995; 36 (02) 239-244 , discussion 244–245
  • 8 Ono K, Oishi H, Tanoue S. et al. Direct carotid-cavernous fistulas occurring during neurointerventional procedures. Interv Neuroradiol 2016; 22 (01) 91-96
  • 9 Kwon HJ, Jin SC. Spontaneous healing of iatrogenic direct carotid cavernous fistula. Interv Neuroradiol 2012; 18 (02) 187-190
  • 10 Tsuji Y, Miki T, Kakita H, Sato K, Yoshida T, Shimizu F. Mechanical thrombectomy for large vessel occlusion via the transbrachial approach: case series. Neurointervention 2020; 15 (02) 89-95
  • 11 Akpinar SH, Gelener P, Kaymakamzade B. Complications of endovascular treatment in acute stroke patients: results from a tertiary referral center. Int J Stroke 2014; 9: 88-88
  • 12 Alan N, Nwachuku E, Jovin TJ, Jankowitz BT, Jadhav AP, Ducruet AF. Management of iatrogenic direct carotid cavernous fistula occurring during endovascular treatment of stroke. World Neurosurg 2017; 100: 710.e15-710.e20

Address for correspondence

Eiichi Ishikawa, MD, PhD
Department of Neurosurgery, Faculty of Medicine, University of Tsukuba
Tsukuba, Ibaraki, 305-8575
Japan   

Publication History

Article published online:
19 October 2022

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  • References

  • 1 Matsumoto H, Nishiyama H, Takemoto H, Tetsuo Y, Nakao N. Carotid-cavernous fistula caused by vessel injury while withdrawing a stent retriever during mechanical thrombectomy for acute ischemic stroke: a case report. J Neuroendovasc Therapy 2018; 12 (05) 235-240
  • 2 Kurashiki Y, Hanaoka M, Sato K. et al. Occurrence of direct carotid-cavernous fistula during mechanical thrombectomy for middle cerebral artery occlusion. Tokushima Red Cross Hosp Med J 2019; 24: 82-89
  • 3 Sheinberg DL, Brunet MC, Chen SH, Luther E, Starke RM. Iatrogenic direct carotid-cavernous fistula following mechanical thrombectomy: a case report and review of the literature. Cureus 2020; 12 (04) e7524
  • 4 Ryu CW, Lee CY, Koh JS, Choi SK, Kim EJ. Vascular perforation during coil embolization of an intracranial aneurysm: the incidence, mechanism, and clinical outcome. Neurointervention 2011; 6 (01) 17-22
  • 5 Bourcier R, Goyal M, Liebeskind DS. et al; HERMES Trialists Collaboration. Association of time from stroke onset to groin puncture with quality of reperfusion after mechanical thrombectomy: a meta-analysis of individual patient data from 7 randomized clinical trials. JAMA Neurol 2019; 76 (04) 405-411
  • 6 Henderson AD, Miller NR. Carotid-cavernous fistula: current concepts in aetiology, investigation, and management. Eye (Lond) 2018; 32 (02) 164-172
  • 7 Lewis AI, Tomsick TA, Tew Jr JM. Management of 100 consecutive direct carotid-cavernous fistulas: results of treatment with detachable balloons. Neurosurgery 1995; 36 (02) 239-244 , discussion 244–245
  • 8 Ono K, Oishi H, Tanoue S. et al. Direct carotid-cavernous fistulas occurring during neurointerventional procedures. Interv Neuroradiol 2016; 22 (01) 91-96
  • 9 Kwon HJ, Jin SC. Spontaneous healing of iatrogenic direct carotid cavernous fistula. Interv Neuroradiol 2012; 18 (02) 187-190
  • 10 Tsuji Y, Miki T, Kakita H, Sato K, Yoshida T, Shimizu F. Mechanical thrombectomy for large vessel occlusion via the transbrachial approach: case series. Neurointervention 2020; 15 (02) 89-95
  • 11 Akpinar SH, Gelener P, Kaymakamzade B. Complications of endovascular treatment in acute stroke patients: results from a tertiary referral center. Int J Stroke 2014; 9: 88-88
  • 12 Alan N, Nwachuku E, Jovin TJ, Jankowitz BT, Jadhav AP, Ducruet AF. Management of iatrogenic direct carotid cavernous fistula occurring during endovascular treatment of stroke. World Neurosurg 2017; 100: 710.e15-710.e20

Zoom Image
Fig. 1 Mechanical thrombectomy: (A, B) Left ICAG revealing a left M2 proximal occlusion. (C) The microcatheter was advanced over a micro-guidewire. (D, arrow) The shape of the microcatheter changed significantly in the syphon portion of the ICA. (E, arrow) The body of the microcatheter perforated the ICA wall and went into the cavernous sinus. (F, G) Left ICAG revealed a direct CCF. Shunt flow was abundant and ascending blood flow to the brain diminished. This complication halted the thrombectomy.
Zoom Image
Fig. 2 The first direct CCF treatment: (A, B) ICAG before the treatment: a fistula is visible in the posterior part of the ICA cavernous segment. Dangerous draining veins, including the left SOV, SMCV, SPS, and inter-CS, were occluded. (C, D) ICAG after treatment: shunt flow reduction was achieved and distal flow is visible.
Zoom Image
Fig. 3 The second direct CCF treatment: (A, B) ICAG before the treatment: a thin inter-CS is clearly seen. We occluded the inter-CS and left inferior petrosal sinus with a coil. (C, D) ICAG after treatment: the direct CCF is diminished with only a small hollow at the fistula. Ascending flow to the brain was recovered.