Partially thrombosed giant basilar artery aneurysm with attenuated contrast enhancement of the intraluminal thrombus on vessel wall MRI after flow diversion treatment: illustrative case

So Matsukawa Departments of Neurosurgery and

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Akira Ishii Departments of Neurosurgery and

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Yasutaka Fushimi Diagnostic Imaging and Nuclear Medicine, Kyoto University Graduate School of Medicine, Faculty of Medicine, Kyoto, Japan

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Yu Abekura Departments of Neurosurgery and

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Takashi Nagahori Departments of Neurosurgery and

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Takayuki Kikuchi Departments of Neurosurgery and

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Masakazu Okawa Departments of Neurosurgery and

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Yukihiro Yamao Departments of Neurosurgery and

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Natsuhi Sasaki Departments of Neurosurgery and

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Hirofumi Tsuji Departments of Neurosurgery and

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Ryo Akiyama Departments of Neurosurgery and

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Susumu Miyamoto Departments of Neurosurgery and

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BACKGROUND

The effect of vessel wall magnetic resonance imaging (VW-MRI) enhancement in partially thrombosed aneurysms has previously indicated aneurysmal instability and a rupture risk. However, whether the contrast effect of the wall changes before or after flow diversion treatment is still under investigation.

OBSERVATIONS

The authors report a case of a partially thrombosed basilar artery aneurysm that increased in size over a short period, worsened brainstem compression symptoms, and was treated with a flow diverter stent with good results. In this case, VW-MRI after surgery showed a reduced contrast effect on the intraluminal thrombus within the aneurysm. The aneurysm thrombosed and markedly regressed over the next 5 months, with remarkable improvement in the brainstem compression symptoms.

LESSONS

This finding on VW-MRI may indicate an attenuation of neovascularization in the thrombus wall and be a sign of aneurysm stabilization.

ABBREVIATIONS

BA = basilar artery; DANTE = delay alternating with nutation for tailored excitation; FRED = flow-redirection endoluminal device; MRI = magnetic resonance imaging; PCA = posterior cerebral artery; POD = postoperative day; VA = vertebral artery; VW-MRI = vessel wall magnetic resonance imaging

BACKGROUND

The effect of vessel wall magnetic resonance imaging (VW-MRI) enhancement in partially thrombosed aneurysms has previously indicated aneurysmal instability and a rupture risk. However, whether the contrast effect of the wall changes before or after flow diversion treatment is still under investigation.

OBSERVATIONS

The authors report a case of a partially thrombosed basilar artery aneurysm that increased in size over a short period, worsened brainstem compression symptoms, and was treated with a flow diverter stent with good results. In this case, VW-MRI after surgery showed a reduced contrast effect on the intraluminal thrombus within the aneurysm. The aneurysm thrombosed and markedly regressed over the next 5 months, with remarkable improvement in the brainstem compression symptoms.

LESSONS

This finding on VW-MRI may indicate an attenuation of neovascularization in the thrombus wall and be a sign of aneurysm stabilization.

ABBREVIATIONS

BA = basilar artery; DANTE = delay alternating with nutation for tailored excitation; FRED = flow-redirection endoluminal device; MRI = magnetic resonance imaging; PCA = posterior cerebral artery; POD = postoperative day; VA = vertebral artery; VW-MRI = vessel wall magnetic resonance imaging

In partially thrombosed aneurysms, high-resolution vessel wall magnetic resonance imaging (VW-MRI) has been used to evaluate the aneurysm wall, and the wall contrast effect is known to indicate aneurysmal instability and rupture risk.1 However, VW-MRI findings before and after flow diversion treatment are still under investigation.2 Here, using the delay alternating with nutation for tailored excitation (DANTE) T1-SPACE (sampling perfection with application-optimized contrasts using different flip angle evolutions), a VW-MRI method, we confirmed that the wall contrast effect in a partially thrombosed aneurysm was attenuated after flow diverter (FD) stent implantation.

Illustrative Case

A 71-year-old male presented with ataxic gait disturbance as the chief complaint. Head magnetic resonance imaging (MRI) revealed a mass compressing the brainstem with surrounding edema (Fig. 1A). VW-MRI (DANTE T1-SPACE) showed continuity with the basilar artery (BA), leading to the diagnosis of a partially thrombosed giant BA aneurysm. Blood flow within the aneurysm was minimal, and most of the aneurysm was considered thrombosed (Fig. 1B and C). In addition, contrast enhancement of the intraluminal thrombus within the aneurysm was observed (Fig. 2A–C). Cerebral angiography showed the same findings as the MRI, with only a small portion of the BA aneurysm visualized (Fig. 1H and I).

FIG. 1
FIG. 1

Axial fluid-attenuated inversion recovery (FLAIR) magnetic resonance imaging (MRI) (A) at the initial examination showing a mass compressing the brainstem with surrounding edema. Sagittal (B) and axial (C) contrast-enhanced delay alternating with nutation for tailored excitation (DANTE) T1-SPACE (sampling perfection with application-optimized contrasts using different flip angle evolutions) at the initial examination showing a giant partially thrombosed basilar artery (BA) aneurysm compressing the brainstem. The blood-flow lumen of the aneurysm, which was contiguous with the BA, was very small, and most of it was thrombosed. Axial FLAIR MRI (D) 1 month after the initial visit showing increased mass effect on the brainstem and worsening edematous changes. Axial FLAIR MRI (E) 5 months after flow diversion treatment showing prominent shrinkage of the aneurysm and improvement in edematous changes. Sagittal (F) and axial (G) contrast-enhanced DANTE T1-SPACE 5 months after flow diversion treatment showing a prominent reduction in the thrombosed area within the aneurysm. Anteroposterior (H) and lateral (I) views of preoperative vertebral angiogram showing only a small portion of the thrombosed aneurysm as the intra-aneurysmal lumen. Three-dimensional rotational angiography (J) showing the flow-redirection endoluminal device (FRED) is placed from the left posterior cerebral artery (PCA) P1–2 junction to the BA and is fully open. Lateral vertebral angiogram (K) 5 months after flow diversion treatment showing complete occlusion of the aneurysm.

FIG. 2
FIG. 2

Sagittal nonenhanced (A) and contrast-enhanced (B) DANTE T1-SPACE at the initial examination showing the contrast effect on the intraluminal thrombus within the aneurysm (white arrowheads). A schema (C) of the image is shown in panel B. The white arrowheads indicate an intra-aneurysmal thrombus in contact with the blood-flow cavity of the aneurysm, which is referred to as an “intraluminal thrombus.” The yellow marker indicates the contrast effect of the intraluminal thrombus. Sagittal nonenhanced (D) and contrast-enhanced (E) DANTE T1-SPACE on postoperative day 1 showing attenuated wall enhancement of the intraluminal thrombus within the aneurysm (white arrowheads). A schema (F) of the image is shown in panel E. The contrast effect (yellow marker) of the intraluminal thrombus, indicated by the white arrowheads, has attenuated after FD implantation. Sagittal nonenhanced (G) and contrast-enhanced (H) DANTE T1-SPACE 3 weeks after surgery showing persistent wall enhancement attenuation of the intraluminal thrombus within the aneurysm (white arrowheads).

Treatment with the placement of an FD stent was planned, and dual antiplatelet therapy (aspirin 100 mg/day and clopidogrel 75 mg/day) was started 2 weeks prior to the surgery. Four days before the scheduled surgery, the patient presented to the emergency department with left upper- and lower-extremity paralysis (Manual Muscle Test 2/5), dysarthria, and dysphagia. MRI showed worsening of the mass effect on the brainstem (Fig. 1D). Steroids (prednisolone 30 mg/day) and glycerol were initiated to reduce edema. Endovascular treatment was performed as planned. With the patient under general anesthesia, an 8-Fr sheath was placed in the right common femoral artery. An 8-Fr guiding catheter was then placed at the origin of the right vertebral artery (VA) and advanced into the intracranial VA using a 6-Fr SOFIASELECT (MicroVention). A Headway27 microcatheter (MicroVention) and Traxcess guidewire (MicroVention) were used to guide to the left posterior cerebral artery (PCA) P2 segment. Additionally, a Headway Duo microcatheter (MicroVention) was guided into the aneurysm. A flow-redirection endoluminal device (FRED; 3.5 × 22 mm, MicroVention) was placed from the left PCA P1–2 junction to the BA through the Headway27 (Fig. 1J). No adjunctive coils were used after FRED implantation because the aneurysm had a small blood-flow lumen. Symptoms gradually improved from postoperative day (POD) 1, and steroids were tapered off and discontinued on POD20. Contrast-enhanced VW-MRI performed on POD1 (Fig. 2D–F) and 3 weeks postoperatively (Fig. 2G and H) showed reduced contrast enhancement of the intraluminal thrombus within the aneurysm. On POD30, the patient was transferred to a rehabilitation hospital with mild paralysis of the left upper extremity (modified Rankin scale score 2). Follow-up cerebral angiography 5 months after treatment showed complete occlusion of the aneurysm (Fig. 1K). Furthermore, MRI showed a significant reduction in the thrombus within the aneurysm and reduced mass effect on the brainstem (Fig. 1E–G). Clopidogrel was discontinued, and only aspirin was continued. The paralytic symptoms resolved almost completely, and the patient became an outpatient.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

Giant (≥25 mm) intracranial aneurysms are a unique subcategory of cerebral aneurysms with a poor natural history and technically demanding treatment options.3,4 Direct surgery results for giant thrombosed aneurysms have been poor, and aneurysms in the posterior circulation region have been considered a poor prognostic factor.5 Some giant aneurysms in the posterior circulation progressively and irreversibly enlarge, causing neurological deficits due to brainstem compression.5 The treatment goal is not only to prevent future hemorrhagic events but also to alleviate the associated mass effect and compression symptoms.4 Treatment strategies for these uncommon intracranial aneurysms remain a matter of substantial debate because evidence from large clinical trials is lacking.4 Recent reports have demonstrated the flow diversion efficacy for giant cerebral aneurysms in the posterior circulation.4,6 However, a significantly higher risk of perforating branch infarction compared with that in anterior circulation aneurysms has also been shown.7

Approximately 50% of giant cerebral aneurysms show thrombosis within the aneurysm.8 The presence of a partial thrombosis has been identified as a clinical biomarker for aneurysm histological findings, suggesting instability and rupture risk.1 Partially thrombosed aneurysms are related to subacute or chronic dissections, repeated intramural hematomas, proliferating vasa vasorum, and the triggering of inflammatory mechanisms.9,10 Endoluminal implants that reduce and redirect blood flow away from the aneurysm sac can diminish the pulsation phenomenon and induce steady intrasaccular thrombosis.4 Similar to the wound-healing mechanism, the biotransformation and organization of the intrasaccular thrombus into fibrous scar tissue allow the aneurysmal structure to be reduced and eventually resorbed to some extent.11 In the present case, we decided to implant an FD stent to stabilize the growing thrombosed aneurysm. In fact, FD stent implantation stopped aneurysmal enlargement and further reduced the size of the giant thrombosed BA aneurysm, which showed a tendency to increase in a short period, suggesting that the decrease in flow within the thrombosed aneurysm itself may have triggered the healing mechanism.

Wall-enhancement patterns of thrombosed intracranial aneurysms on MRI are recognized as a clinical alert sign that indicates unstable behavior.12 Partial or complete inner wall enhancement correlates with neovascularization of the inner wall layer and adjacent thrombus.1

Furthermore, it has been suggested that the change in contrast effect on VW-MRI before and after flow diversion treatment may indicate a potential biomarker of healing,2 but the details are still under investigation, and the relationship with steroids is unknown.

In this case, preoperative contrast-enhanced VW-MRI confirmed the contrast effect on the intraluminal thrombus within the aneurysm. We observed a reduction in the contrast effect of the intraluminal thrombus within the aneurysm after FD stent implantation. The fact that such a finding was observed the day after the procedure is novel. This finding on VW-MRI may indicate that neovascularization of the thrombus wall, developed by repeated dissection of the intra-aneurysmal lumen wall caused by hemodynamic injury, was attenuated. This may be a sign of stabilization of the intrasaccular thrombosis and may lead to negative remodeling of the aneurysm.

Because of its potential as a biomarker of healing, we routinely perform contrast-enhanced VW-MRI in patients after FD stent implantation, and we believe that its decreased invasiveness compared with cerebral angiography justifies its frequent examination. Whether the lack of contrast attenuation on posttreatment VW-MRI is an indicator of a poor prognosis or whether steroid use is a confounding factor needs to be further investigated in more cases.

Lessons

In partially thrombosed aneurysms, attenuated wall enhancement of the intraluminal thrombus on contrast-enhanced VW-MRI after flow diversion may be a sign of aneurysm stabilization.

Acknowledgments

We are grateful to Yuta Urushibata of Siemens Japan K.K. and John Grinstead and Sinyeob Ahn of Siemens Healthineers for providing the prototype sequence.

Author Contributions

Conception and design: Ishii, Matsukawa, Sasaki. Acquisition of data: Matsukawa, Fushimi, Nagahori, Yamao, Sasaki, Tsuji. Analysis and interpretation of data: Matsukawa, Abekura, Kikuchi, Okawa. Drafting of the article: Matsukawa, Fushimi. Critically revising the article: Ishii, Matsukawa, Fushimi, Kikuchi, Okawa, Miyamoto. Reviewed submitted version of the manuscript: Ishii, Matsukawa, Kikuchi, Okawa, Yamao, Sasaki, Akiyama. Approved the final version of the manuscript on behalf of all authors: Ishii. Study supervision: Ishii, Miyamoto.

References

  • 1

    Sato T, Matsushige T, Chen B, et al. Wall contrast enhancement of thrombosed intracranial aneurysms at 7T MRI. AJNR Am J Neuroradiol. 2019;40(7):11061111.

  • 2

    Raz E, Goldman-Yassen A, Derman A, Derakhshani A, Grinstead J, Dehkharghani S. Vessel wall imaging with advanced flow suppression in the characterization of intracranial aneurysms following flow diversion with Pipeline embolization device. J Neurointerv Surg. 2022;14(12):12641269.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Cagnazzo F, Mantilla D, Rouchaud A, et al. Endovascular treatment of very large and giant intracranial aneurysms: comparison between reconstructive and deconstructive techniques—a meta-analysis. AJNR Am J Neuroradiol. 2018;39(5):852858.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Sirakova K, Penkov M, Matanov S, et al. Progressive volume reduction and long-term aneurysmal collapse following flow diversion treatment of giant and symptomatic cerebral aneurysms. Front Neurol. 2022;13:972599.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Vannemreddy PS, Nourbakhsh A, Nanda A. Evaluation of the prognostic indicators of giant intracranial aneurysms. Skull Base. 2011;21(1):3746.

  • 6

    Piano M, Valvassori L, Lozupone E, Pero G, Quilici L, Boccardi E. FRED Italian Registry: a multicenter experience with the flow re-direction endoluminal device for intracranial aneurysms. J Neurosurg. Published online May 10, 2019. doi: 10.3171/2019.1.JNS183005.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke. 2013;44(2):442447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Whittle IR, Dorsch NW, Besser M. Spontaneous thrombosis in giant intracranial aneurysms. J Neurol Neurosurg Psychiatry. 1982;45(11):10401047.

  • 9

    Alvarez H. Etiology of giant aneurysms and their treatment. AJNR Am J Neuroradiol. 2009;30(1):E8E10, author reply E9–E10.

  • 10

    Ferns SP, van Rooij WJ, Sluzewski M, van den Berg R, Majoie CB. Partially thrombosed intracranial aneurysms presenting with mass effect: long-term clinical and imaging follow-up after endovascular treatment. AJNR Am J Neuroradiol. 2010;31(7):11971205.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Ngoepe MN, Frangi AF, Byrne JV, Ventikos Y Thrombosis in cerebral aneurysms and the computational modeling thereof: a review. Front Physiol. 2018;9:306.

  • 12

    Iihara K, Murao K, Yamada N, et al. Growth potential and response to multimodality treatment of partially thrombosed large or giant aneurysms in the posterior circulation. Neurosurgery. 2008;63(5):832842, discussion 842–844.

    • PubMed
    • Search Google Scholar
    • Export Citation
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  • Expand
  • FIG. 1

    Axial fluid-attenuated inversion recovery (FLAIR) magnetic resonance imaging (MRI) (A) at the initial examination showing a mass compressing the brainstem with surrounding edema. Sagittal (B) and axial (C) contrast-enhanced delay alternating with nutation for tailored excitation (DANTE) T1-SPACE (sampling perfection with application-optimized contrasts using different flip angle evolutions) at the initial examination showing a giant partially thrombosed basilar artery (BA) aneurysm compressing the brainstem. The blood-flow lumen of the aneurysm, which was contiguous with the BA, was very small, and most of it was thrombosed. Axial FLAIR MRI (D) 1 month after the initial visit showing increased mass effect on the brainstem and worsening edematous changes. Axial FLAIR MRI (E) 5 months after flow diversion treatment showing prominent shrinkage of the aneurysm and improvement in edematous changes. Sagittal (F) and axial (G) contrast-enhanced DANTE T1-SPACE 5 months after flow diversion treatment showing a prominent reduction in the thrombosed area within the aneurysm. Anteroposterior (H) and lateral (I) views of preoperative vertebral angiogram showing only a small portion of the thrombosed aneurysm as the intra-aneurysmal lumen. Three-dimensional rotational angiography (J) showing the flow-redirection endoluminal device (FRED) is placed from the left posterior cerebral artery (PCA) P1–2 junction to the BA and is fully open. Lateral vertebral angiogram (K) 5 months after flow diversion treatment showing complete occlusion of the aneurysm.

  • FIG. 2

    Sagittal nonenhanced (A) and contrast-enhanced (B) DANTE T1-SPACE at the initial examination showing the contrast effect on the intraluminal thrombus within the aneurysm (white arrowheads). A schema (C) of the image is shown in panel B. The white arrowheads indicate an intra-aneurysmal thrombus in contact with the blood-flow cavity of the aneurysm, which is referred to as an “intraluminal thrombus.” The yellow marker indicates the contrast effect of the intraluminal thrombus. Sagittal nonenhanced (D) and contrast-enhanced (E) DANTE T1-SPACE on postoperative day 1 showing attenuated wall enhancement of the intraluminal thrombus within the aneurysm (white arrowheads). A schema (F) of the image is shown in panel E. The contrast effect (yellow marker) of the intraluminal thrombus, indicated by the white arrowheads, has attenuated after FD implantation. Sagittal nonenhanced (G) and contrast-enhanced (H) DANTE T1-SPACE 3 weeks after surgery showing persistent wall enhancement attenuation of the intraluminal thrombus within the aneurysm (white arrowheads).

  • 1

    Sato T, Matsushige T, Chen B, et al. Wall contrast enhancement of thrombosed intracranial aneurysms at 7T MRI. AJNR Am J Neuroradiol. 2019;40(7):11061111.

  • 2

    Raz E, Goldman-Yassen A, Derman A, Derakhshani A, Grinstead J, Dehkharghani S. Vessel wall imaging with advanced flow suppression in the characterization of intracranial aneurysms following flow diversion with Pipeline embolization device. J Neurointerv Surg. 2022;14(12):12641269.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Cagnazzo F, Mantilla D, Rouchaud A, et al. Endovascular treatment of very large and giant intracranial aneurysms: comparison between reconstructive and deconstructive techniques—a meta-analysis. AJNR Am J Neuroradiol. 2018;39(5):852858.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Sirakova K, Penkov M, Matanov S, et al. Progressive volume reduction and long-term aneurysmal collapse following flow diversion treatment of giant and symptomatic cerebral aneurysms. Front Neurol. 2022;13:972599.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Vannemreddy PS, Nourbakhsh A, Nanda A. Evaluation of the prognostic indicators of giant intracranial aneurysms. Skull Base. 2011;21(1):3746.

  • 6

    Piano M, Valvassori L, Lozupone E, Pero G, Quilici L, Boccardi E. FRED Italian Registry: a multicenter experience with the flow re-direction endoluminal device for intracranial aneurysms. J Neurosurg. Published online May 10, 2019. doi: 10.3171/2019.1.JNS183005.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke. 2013;44(2):442447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Whittle IR, Dorsch NW, Besser M. Spontaneous thrombosis in giant intracranial aneurysms. J Neurol Neurosurg Psychiatry. 1982;45(11):10401047.

  • 9

    Alvarez H. Etiology of giant aneurysms and their treatment. AJNR Am J Neuroradiol. 2009;30(1):E8E10, author reply E9–E10.

  • 10

    Ferns SP, van Rooij WJ, Sluzewski M, van den Berg R, Majoie CB. Partially thrombosed intracranial aneurysms presenting with mass effect: long-term clinical and imaging follow-up after endovascular treatment. AJNR Am J Neuroradiol. 2010;31(7):11971205.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Ngoepe MN, Frangi AF, Byrne JV, Ventikos Y Thrombosis in cerebral aneurysms and the computational modeling thereof: a review. Front Physiol. 2018;9:306.

  • 12

    Iihara K, Murao K, Yamada N, et al. Growth potential and response to multimodality treatment of partially thrombosed large or giant aneurysms in the posterior circulation. Neurosurgery. 2008;63(5):832842, discussion 842–844.

    • PubMed
    • Search Google Scholar
    • Export Citation

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