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Wall permeability on magnetic resonance imaging is associated with intracranial aneurysm symptoms and wall enhancement

  • Magnetic Resonance
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European Radiology Aims and scope Submit manuscript

A Commentary to this article was published on 19 January 2024

Abstract

Objectives

Wall remodeling and inflammation accompany symptomatic unruptured intracranial aneurysms (UIAs). The volume transfer constant (Ktrans) of dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) reflects UIA wall permeability. Aneurysmal wall enhancement (AWE) on vessel wall MRI (VWI) is associated with inflammation. We hypothesized that Ktrans is related to symptomatic UIAs and AWE.

Methods

Consecutive patients with UIAs were prospectively recruited for 3-T DCE-MRI and VWI from January 2018 to March 2023. UIAs were classified as asymptomatic and symptomatic if associated with sentinel headache or oculomotor nerve palsy. Ktrans and AWE were assessed on DCE-MRI and VWI, respectively. AWE was evaluated using the AWE pattern and wall enhancement index (WEI). Spearman’s correlation coefficient and univariate and multivariate analyses were used to assess correlations between parameters.

Results

We enrolled 82 patients with 100 UIAs (28 symptomatic and 72 asymptomatic). The median Ktrans (2.1 versus 0.4 min−1; p < 0.001) and WEI (1.5 versus 0.4; p < 0.001) were higher for symptomatic aneurysms than for asymptomatic aneurysms. Ktrans (odds ratio [OR]: 1.60, 95% confidence interval [95% CI]: 1.01–2.52; p = 0.04) and WEI (OR: 3.31, 95% CI: 1.05–10.42; p = 0.04) were independent risk factors for symptomatic aneurysms. Ktrans was positively correlated with WEI (Spearman’s coefficient of rank correlation (rs) = 0.41, p < 0.001). The combination of Ktrans and WEI achieved an area under the curve of 0.81 for differentiating symptomatic from asymptomatic aneurysms.

Conclusions

Ktrans may be correlated with symptomatic aneurysms and AWE. Ktrans and WEI may provide an additional value than the PHASES score for risk stratification of UIAs.

Clinical relevance statement

The volume transfer constant (Ktrans) from DCE-MRI perfusion is associated with symptomatic aneurysms and provides additional value above the clinical PHASES score for risk stratification of intracranial aneurysms.

Key Points

• The volume transfer constant is correlated with intracranial aneurysm symptoms and aneurysmal wall enhancement.

• Dynamic contrast-enhanced and vessel wall MRI facilitates understanding of the pathophysiological characteristics of intracranial aneurysm walls.

• The volume transfer constant and wall enhancement index perform better than the traditional PHASES score in differentiating symptomatic aneurysms.

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Abbreviations

AUC:

Area under the curve

AWE:

Aneurysmal wall enhancement

AWEP:

Aneurysmal wall enhancement pattern

CI:

Confidence interval

DCE-MRI:

Dynamic contrast-enhanced magnetic resonance imaging

FOV:

The field of view

IAs:

Intracranial aneurysms

K trans :

The volume transfer constant

OR:

Odds ratio

ROI:

Region of interest

Rs:

Spearman’s coefficient of rank correlation

SAH:

Subarachnoid hemorrhage

SD:

Standard deviation

SI:

Signal intensity

SPACE:

Fast-spin-echo with variable flip angle trains

TOF MRA:

Time-of-flight magnetic resonance angiography

UIAs:

Unruptured intracranial aneurysms

VFA:

Variable flip angle

VIBE:

Volumetric interpolated breathhold

VIF:

Variance inflation factor

VOI:

Volume of interest

VWI:

Vessel wall magnetic resonance imaging

WEI:

Wall enhancement index

References

  1. Vernooij MW, Ikram MA, Tanghe HL et al (2007) Incidental findings on brain MRI in the general population. N Engl J Med 357:1821–1828

    Article  CAS  PubMed  Google Scholar 

  2. Wang Y, Cheng M, Liu S et al (2022) Shape related features of intracranial aneurysm are associated with rupture status in a large Chinese cohort. Journal of neurointerventional surgery 14:252–256

    Article  PubMed  Google Scholar 

  3. Juvela S (2022) PHASES score and treatment scoring with cigarette smoking in the long-term prediction of rupturing of unruptured intracranial aneurysms. J Neurosurg 136:156–162

    Article  PubMed  Google Scholar 

  4. Wermer MJH, van der Schaaf IC, Algra A, Rinkel GJE (2007) Risk of rupture of unruptured intracranial aneurysms in relation to patient and aneurysm characteristics: an updated meta-analysis. Stroke 38:1404–1410

    Article  PubMed  Google Scholar 

  5. Fu Q, Wang Y, Zhang Y et al (2021) Qualitative and quantitative wall enhancement on magnetic resonance imaging is associated with symptoms of unruptured intracranial aneurysms. Stroke 52:213–222

    Article  PubMed  Google Scholar 

  6. Morel S, Bijlenga P, Kwak BR (2022) Intracranial aneurysm wall (in)stability-current state of knowledge and clinical perspectives. Neurosurg Rev 45:1233–1253

    Article  PubMed  Google Scholar 

  7. Frösen J (2014) Smooth muscle cells and the formation, degeneration, and rupture of saccular intracranial aneurysm wall–a review of current pathophysiological knowledge. Transl Stroke Res 5:347–356

    Article  PubMed  Google Scholar 

  8. Zhong W, Su W, Li T et al (2021) Aneurysm wall enhancement in unruptured intracranial aneurysms: a histopathological evaluation. J Am Heart Assoc 10:e018633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cantrell CG, Vakil P, Jeong Y, Ansari SA, Carroll TJ (2017) Diffusion-compensated tofts model suggests contrast leakage through aneurysm wall. Magn Reson Med 78:2388–2398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Qi H, Liu X, Liu P et al (2019) Complementary roles of dynamic contrast-enhanced MR imaging and postcontrast vessel wall imaging in detecting high-risk intracranial aneurysms. AJNR Am J Neuroradiol 40:490–496

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Edjlali M, Guédon A, Ben Hassen W et al (2018) Circumferential thick enhancement at vessel wall MRI has high specificity for intracranial aneurysm instability. Radiology 289:181–187

    Article  PubMed  Google Scholar 

  12. Vakil P, Ansari SA, Cantrell CG et al (2015) Quantifying intracranial aneurysm wall permeability for risk assessment using dynamic contrast-enhanced MRI: a pilot study. AJNR Am J Neuroradiol 36:953–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tóth A (2023) Wall enhancement in stable aneurysms needs to be understood first to be able to identify instable and culprit aneurysms. Eur Radiol 33:4915–4917

    Article  PubMed  Google Scholar 

  14. Molenberg R, Aalbers MW, Appelman APA, Uyttenboogaart M, van Dijk JMC (2021) Intracranial aneurysm wall enhancement as an indicator of instability: a systematic review and meta-analysis. Eur J Neurol 28:3837–3848

    Article  PubMed  PubMed Central  Google Scholar 

  15. Matsushige T, Shimonaga K, Ishii D et al (2019) Vessel wall imaging of evolving unruptured intracranial aneurysms. Stroke 50:1891–1894

    Article  PubMed  Google Scholar 

  16. Greving JP, Wermer MJH, Brown RD et al (2014) Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. The Lancet Neurology 13:59–66

    Article  PubMed  Google Scholar 

  17. O’brien RM (2007) Quality & Quantity. A caution regarding rules of thumb for variance inflation factors 41:673–690

    Google Scholar 

  18. Ball MJ (1975) Pathogenesis of the “sentinel headache” preceding berry aneurysm rupture. Can Med Assoc J 112:78–79

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Nakagawa D, Kudo K, Awe O et al (2018) Detection of microbleeds associated with sentinel headache using MRI quantitative susceptibility mapping: pilot study. J Neurosurg. https://doi.org/10.3171/2018.2.JNS1884:1-7

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wang Y, Sun J, Li R et al (2022) Increased aneurysm wall permeability colocalized with low wall shear stress in unruptured saccular intracranial aneurysm. J Neurol 269:2715–2719

    Article  CAS  PubMed  Google Scholar 

  21. Peng F, Niu H, Feng X et al (2023) Aneurysm wall enhancement, atherosclerotic proteins, and aneurysm size may be related in unruptured intracranial fusiform aneurysms. Eur Radiol 33:4918–4926

    Article  CAS  PubMed  Google Scholar 

  22. Kang H, Tian D-C, Yang X et al (2022) A randomized controlled trial of statins to reduce inflammation in unruptured cerebral aneurysms. JACC Cardiovasc Imaging 15:1668–1670

    Article  PubMed  Google Scholar 

  23. Quan K, Song J, Yang Z et al (2019) Validation of wall enhancement as a new imaging biomarker of unruptured cerebral aneurysm. Stroke 50:1570–1573

    Article  PubMed  Google Scholar 

  24. Meng H, Tutino VM, Xiang J, Siddiqui A (2014) High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. AJNR Am J Neuroradiol 35:1254–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Etminan N, Rinkel GJ (2016) Unruptured intracranial aneurysms: development, rupture and preventive management. Nat Rev Neurol 12:699–713

    Article  PubMed  Google Scholar 

  26. Zhu C, Wang X, Eisenmenger L et al (2020) Wall enhancement on black-blood MRI is independently associated with symptomatic status of unruptured intracranial saccular aneurysm. Eur Radiol 30:6413–6420

    Article  PubMed  Google Scholar 

  27. Peng F, Fu M, Xia J et al (2022) Quantification of aneurysm wall enhancement in intracranial fusiform aneurysms and related predictors based on high-resolution magnetic resonance imaging: a validation study. Ther Adv Neurol Disord 15:17562864221105342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ge P, Liu C, Chan L et al (2022) High-dimensional immune profiling by mass cytometry revealed the circulating immune cell landscape in patients with intracranial aneurysm. Front Immunol 13:922000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Chalouhi N, Hoh BL, Hasan D (2013) Review of cerebral aneurysm formation, growth, and rupture. Stroke 44:3613–3622

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Jinxia Zhu and Feifei Qu of Siemens Healthineers Ltd for supporting MRI sequence debugging, data post-processing, and article polishing.

We sincerely thank all the patients and healthcare workers who participated in this study.

Funding

This study has received funding from the National Natural Science Foundation of China (Grant 82202105) and the Joint construction project in Henan Province (Grant LHGJ20220406). Chengcheng Zhu was supported by grants R01HL162743 and R00HL136883 from the United States National Institute of Health (NIH).

Author information

Authors and Affiliations

  1. Department of Magnetic Resonance, The First Affiliated Hospital of Zhengzhou University, 1St Construction of E Rd, Two-Seven Districts, Zhengzhou, 450052, China

    Qichang Fu, Yi Zhang, Yong Zhang & Jingliang Cheng

  2. Department of Interventional Neuroradiology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China

    Chao Liu, Jinyi Li & Sheng Guan

  3. Department of Neurosurgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China

    Meng Wang

  4. Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China

    Haiyang Luo

  5. MR Collaboration, Siemens Healthineers Ltd, Beijing, China

    Jinxia Zhu & Feifei Qu

  6. Department of Radiology, University of Washington School of Medicine, Seattle, WA, USA

    Mahmud Mossa-Basha & Chengcheng Zhu

Authors
  1. Qichang Fu
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Corresponding author

Correspondence to Jingliang Cheng.

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Guarantor

The scientific guarantor of this publication is Jingliang Cheng.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

Chunhua Song (a medical statistician from Zhengzhou University) kindly provided statistical advice for this manuscript.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

The approval of the ethics committee of the First Affiliated Hospital of Zhengzhou University was obtained (Ethics No. ss-2018–11).

Study subjects or cohorts overlap

Some study subjects or cohorts have been previously reported in “Qualitative and Quantitative Wall Enhancement on Magnetic Resonance Imaging Is Associated With Symptoms of Unruptured Intracranial Aneurysms. Stroke (1970) 52:213–222” and “Evaluation of the Instability of Intracranial Aneurysms Wall by Dynamic Contrast-enhanced Magnetic Resonance Imaging and Vessel Wall Imaging” by the International Society for Medical Magnetic Resonance Annual Meeting (ISMRM 2022).

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Fu, Q., Zhang, Y., Zhang, Y. et al. Wall permeability on magnetic resonance imaging is associated with intracranial aneurysm symptoms and wall enhancement. Eur Radiol (2024). https://doi.org/10.1007/s00330-023-10548-9

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