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Association of preoperative aneurysmal wall enhancement with relief of chronic headache after surgical clipping of unruptured intracranial aneurysms

  • Magnetic Resonance
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Abstract

Objective

To investigate the association between chronic headache outcome and aneurysmal wall enhancement (AWE) on high-resolution vessel wall imaging (HR-VWI) in patients with unruptured intracranial aneurysms (UIAs) who underwent microsurgical clipping.

Methods

Two hundred seventy-four UIA patients were retrospectively analyzed. Patients were grouped according to presence of AWE. AWE was subclassified as focal or uniform. Clinical and imaging data were recorded. Headache was evaluated using the 10-point numerical rating scale and Headache Impact Test-6 before and 6 months after surgery.

Results

The proportions of patients reporting chronic headache in the no AWE, focal wall enhancement (FWE), and uniform wall enhancement (UWE) groups were 5.7%, 24.8%, and 41.8%, respectively. All patients in the UWE group who reported headache before surgery experienced headache improvement after surgery. Decrease in headache severity was greater in the UWE group than in the FWE group. Multivariate binary logistic regression showed that FWE (odds ratio (OR) 0.490; 95% confidence interval (CI), 0.262–0.917; p = 0.026) and small intraluminal thrombus (OR 0.336; 95% CI, 0.142–0.795; p = 0.013) were independent factors protective against preoperative headache. FWE (OR 0.377; 95% CI, 0.195–0.728; p = 0.004) and small intraluminal thrombus (OR 0.235; 95% CI, 0.088–0.630; p = 0.004) were independent predictors of no headache relief after surgery.

Conclusions

AWE on HR-VWI is associated with relief of chronic headache after surgical clipping in patients with UIAs. Incidence of chronic headache was highest in patients exhibiting UWE. These patients also experienced the greatest improvement in headache after surgical clipping.

Clinical relevance statement

This study revealed that high-resolution vessel wall imaging can demonstrate aneurysmal wall plaque and intraluminal thrombus, which may be prognostic imaging markers for chronic headache in patients with unruptured intracranial aneurysms.

Key Points

• Aneurysmal wall enhancement may be associated with chronic headache.

• Incidence of chronic headache was highest in patients with aneurysms exhibiting uniform wall enhancement.

• Patients with aneurysms exhibiting uniform wall enhancement experienced the greatest improvement in headache after clipping.

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Abbreviations

AWE:

Aneurysmal wall enhancement

CI:

Confidence interval

CNS:

Central nervous system

FWE:

Focal wall enhancement

HAMA:

Hamilton Anxiety Rating Scale

HIT-6:

Headache Impact Test-6

HR-VWI:

High-resolution vessel wall magnetic resonance imaging

mRS:

Modified Rankin scale

NRS:

Numerical rating scale

NSAIDs:

Non-steroidal anti-inflammatory drugs

OR:

Odds ratio

SAH:

Subarachnoid hemorrhage

UIAs:

Unruptured intracranial aneurysms

UWE:

Uniform wall enhancement

References

  1. Vlak MHM, Algra A, Brandenburg R, Rinkel GJE (2011) Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis. Lancet Neurol 10:626–636. https://doi.org/10.1016/S1474-4422(11)70109-0

    Article  PubMed  Google Scholar 

  2. England TN (1998) Unruptured intracranial aneurysms — risk of rupture and risks of surgical intervention. N Engl J Med 339:1725–1733. https://doi.org/10.1056/NEJM199812103392401

    Article  Google Scholar 

  3. Park JH, Kim H, Kim SR et al (2018) Headache outcomes after coil embolization in patients with unruptured intracranial aneurysms: do they get better or worse? A prospective analysis. World Neurosurg 114:e191–e198. https://doi.org/10.1016/j.wneu.2018.02.138

    Article  PubMed  Google Scholar 

  4. Maragkos GA, Cordell S, Gomez-Paz S et al (2020) Flow diversion endovascular treatment improves headaches in patients with unruptured intracranial aneurysms. World Neurosurg 140:e140–e147. https://doi.org/10.1016/j.wneu.2020.04.206

    Article  PubMed  Google Scholar 

  5. Schwedt TJ, Gereau RW, Frey K, Kharasch ED (2011) Headache outcomes following treatment of unruptured intracranial aneurysms: a prospective analysis. Cephalalgia 31:1082–1089. https://doi.org/10.1177/0333102411398155

    Article  PubMed  PubMed Central  Google Scholar 

  6. Dandurand C, Parhar HS, Naji F et al (2019) Headache outcomes after treatment of unruptured intracranial aneurysm a systematic review and meta-analysis. Stroke 50:3628–3631. https://doi.org/10.1161/STROKEAHA.119.026864

    Article  PubMed  Google Scholar 

  7. Kong DS, Hong SC, Jung YJ, Kim JS (2007) Improvement of chronic headache after treatment of unruptured intracranial aneurysms. Headache 47:693–697. https://doi.org/10.1111/j.1526-4610.2006.00630.x

    Article  PubMed  Google Scholar 

  8. 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. https://doi.org/10.1161/STROKEAHA.118.024195

    Article  PubMed  Google Scholar 

  9. Lehman VT, Brinjikji W, Mossa-Basha M et al (2018) Conventional and high-resolution vessel wall MRI of intracranial aneurysms: current concepts and new horizons. J Neurosurg 128:969–981. https://doi.org/10.3171/2016.12.JNS162262

    Article  PubMed  Google Scholar 

  10. 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. https://doi.org/10.1007/s00330-020-07063-6

    Article  PubMed  Google Scholar 

  11. Kwon OK (2019) Headache and aneurysm. Neuroimaging Clin N Am 29:255–260. https://doi.org/10.1016/j.nic.2019.01.004

    Article  PubMed  Google Scholar 

  12. Nichols FT, Mawad M, Mohr JP et al (1990) Focal headache during balloon inflation in the internal carotid and middle cerebral arteries. Stroke 21:555–559. https://doi.org/10.1161/01.STR.21.4.555

    Article  PubMed  Google Scholar 

  13. Li H, Zhang X, Zhang Q-R, Hang C-H (2014) Resolution of migraine-like headache by coil embolization of a primitive trigeminal artery aneurysm. Pain Med 15:1052–1055. https://doi.org/10.1111/pme.12394

    Article  PubMed  Google Scholar 

  14. Arena JE, Hawkes MA, Farez MF et al (2017) Headache and treatment of unruptured intracranial aneurysms. J Stroke Cerebrovasc Dis 26:1098–1103. https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.12.026

    Article  PubMed  Google Scholar 

  15. Gu DQ, Duan CZ, Li XF et al (2013) Effect of endovascular treatment on headache in elderly patients with unruptured intracranial aneurysms. AJNR Am J Neuroradiol 34:1227–1231. https://doi.org/10.3174/ajnr.A3353

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32:50–55. https://doi.org/10.1111/j.2044-8341.1959.tb00467.x

    Article  CAS  PubMed  Google Scholar 

  17. Olesen J (2018) Headache Classification Committee of the International Headache Society (IHS) The International Classification of Headache Disorders, 3rd edition. Cephalalgia 38:1–211. https://doi.org/10.1177/0333102417738202

    Article  Google Scholar 

  18. Heldner MR, Nedelcheva M, Yan X et al (2015) Dynamic changes of intramural hematoma in patients with acute spontaneous internal carotid artery dissection. Int J Stroke 10:887–892. https://doi.org/10.1111/ijs.12553

    Article  PubMed  Google Scholar 

  19. Kosinski M, Bayliss MS, Bjorner JB et al (2003) A six-item short-form survey for measuring headache impact: the HIT-6™. Qual Life Res 12:963–974. https://doi.org/10.1023/A:1026119331193

    Article  CAS  PubMed  Google Scholar 

  20. Zhu C, Wang X, Degnan AJ et al (2018) Wall enhancement of intracranial unruptured aneurysm is associated with increased rupture risk and traditional risk factors. Eur Radiol 28:5019–5026. https://doi.org/10.1007/s00330-018-5522-z

    Article  PubMed  Google Scholar 

  21. Merli E, Rustici A, Gramegna LL et al (2022) Vessel-wall MRI in primary headaches: the role of neurogenic inflammation. Headache 1–8. https://doi.org/10.1111/head.14253

  22. Van Os HJA, Mulder IA, Van Der Schaaf IC et al (2016) Role of atherosclerosis, clot extent, and penumbra volume in headache during ischemic stroke. Neurology 87:1124–1130. https://doi.org/10.1212/WNL.0000000000003092

    Article  CAS  PubMed  Google Scholar 

  23. Mitsias PD, Ramadan NM, Levine SR et al (2006) Factors determining headache at onset of acute ischemic stroke. Cephalalgia 26:150–157. https://doi.org/10.1111/j.1468-2982.2005.01012.x

    Article  CAS  PubMed  Google Scholar 

  24. Shimonaga K, Matsushige T, Ishii D et al (2018) Clinicopathological insights from vessel wall imaging of unruptured intracranial aneurysms. Stroke 49:2516–2529. https://doi.org/10.1161/STROKEAHA.118.021819

    Article  PubMed  Google Scholar 

  25. Rodríguez-Catarino M, Frisén L, Wikholm G et al (2003) Internal carotid artery aneurysms, cranial nerve dysfunction and headache: the role of deformation and pulsation. Neuroradiology 45:236–240. https://doi.org/10.1007/s00234-002-0934-4

    Article  PubMed  Google Scholar 

  26. Iversen HK, Nielsen TH, Olesen J, Tfelt-Hansen P (1990) Arterial responses during migraine headache. Lancet 336:837–839. https://doi.org/10.1016/0140-6736(90)92339-J

    Article  CAS  PubMed  Google Scholar 

  27. Restuccia G, Cavazza A, Boiardi L et al (2012) Small-vessel vasculitis surrounding an uninflamed temporal artery and isolated vasa vasorum vasculitis of the temporal artery: two subsets of giant cell arteritis. Arthritis Rheum 64:549–556. https://doi.org/10.1002/art.33362

    Article  PubMed  Google Scholar 

  28. Masutani EM, Bahrami N, Hsiao A (2020) Deep learning single-frame and multiframe super-resolution for cardiac MRI. Radiology 295:552–561. https://doi.org/10.1148/radiol.2020192173

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Liwen Bianji (Edanz) (www.liwenbianji.cn) for editing the language of this manuscript.

Funding

This study was supported by the National Natural Science Foundation of China (No. 82171311, No. 81801148), Shanghai Excellent Academic Leader Program (No. 21XD1400600), Shanghai Science and Technology Commission Project (No. 23ZR1408700), Clinical Research Plan of SHDC (No. SHDC2020CR2034B, No. SHDC2020CR4033) and ZJ Lab, and CAMS Innovation Fund for Medical Sciences (CIFMS, 2019-I2M-5–008).

Author information

Author notes

  1. Kai Quan, Liuxun Hu, and Shichao Zhang contributed equally; they were first authors.

Authors and Affiliations

  1. Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, 12 Middle Wulumuqi Road, Shanghai, 200040, China

    Kai Quan, Liuxun Hu, Ying Mao & Wei Zhu

  2. National Center for Neurological Disorders, Shanghai, 200040, China

    Kai Quan, Liuxun Hu, Ying Mao & Wei Zhu

  3. Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China

    Kai Quan, Liuxun Hu, Ying Mao & Wei Zhu

  4. Neurosurgical Institute of Fudan University, Shanghai, 200040, China

    Kai Quan, Liuxun Hu, Ying Mao & Wei Zhu

  5. Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, China

    Kai Quan, Liuxun Hu, Ying Mao & Wei Zhu

  6. School of Information Science and Technology, Fudan University, Shanghai, 200433, China

    Shichao Zhang, Yufei Jin & Yu Ma

  7. Key Laboratory of Medical Imaging Computing and Computer Assisted Intervention (MICCAI) of Shanghai, Shanghai, 200032, China

    Shichao Zhang, Yufei Jin & Yu Ma

  8. Department of Radiology, Huashan Hospital, Fudan University, Shanghai, China

    Dongdong Wang

  9. Department of Biostatistics, School of Public Health, Fudan University, Shanghai, 200030, China

    Jianfeng Luo

Authors
  1. Kai Quan
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Corresponding authors

Correspondence to Yu Ma, Ying Mao or Wei Zhu.

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Guarantor

The scientific guarantor of this publication is “Wei Zhu,” and the institution is “Department of Neurosurgery, Huashan Hospital, Fudan University.”

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

“Jianfeng Luo” kindly provided statistical advice for this manuscript.

Informed consent

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

Ethical approval

Institutional Review Board approval was obtained (IRB 2017-D386).

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  • Observational

  • Performed at one institution

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Quan, K., Hu, L., Zhang, S. et al. Association of preoperative aneurysmal wall enhancement with relief of chronic headache after surgical clipping of unruptured intracranial aneurysms. Eur Radiol (2023). https://doi.org/10.1007/s00330-023-10303-0

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