Skip to main content
SpringerLink
Log in

Detection of vessel wall calcifications in vertebral arteries using susceptibility weighted imaging

  • Diagnostic Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Calcification of the brain supplying arteries has been linked to an increased risk for cerebrovascular disease. The purpose of this study was to test the potential of susceptibility weighted MR imaging (SWMR) for the detection of vertebral artery calcifications, based on CT as a reference standard.

Methods

Four hundred seventy-four patients, who had received head CT and 1.5 T MR scans with SWMR, including the distal vertebral artery, between January 2014 and December 2016, were retrospectively evaluated and 389 patients were included. Sensitivity and specificity for the detection of focal calcifications and intra- and interobserver agreement were calculated for SWMR and standard MRI, using CT as a standard of reference. The diameter of vertebral artery calcifications was used to assess correlations between imaging modalities. Furthermore, the degree of vessel stenosis was determined in 30 patients, who had received an additional angiography.

Results

On CT scans, 40 patients showed a total of 52 vertebral artery calcifications. While SWMR reached a sensitivity of 94% (95% CI 84–99%) and a specificity of 97% (95% CI 94–98%), standard MRI yielded a sensitivity of 33% (95% CI 20–46%), and a specificity of 93% (95% CI 90–96%). Linear regression analysis of size measurements confirmed a close correlation between SWMR and CT measurements (R 2 = 0.74, p < 0.001). Compared to standard MRI (ICC = 0.52; CI 0.45–0.59), SWMR showed a higher interobserver agreement for calcification measurements (ICC = 0.84; CI 0.81–0.87).

Conclusions

For detection of distal vertebral artery calcifications, SWMR demonstrates a performance comparable to CT and considerably higher than conventional MRI.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

SWMR:

Susceptibility weighted magnetic resonance

CE:

Imaging contrast enhanced

CTA:

Computed tomography angiography

GRE:

Gradient echo

MRA:

Magnetic resonance angiography

NASCET:

North American Symptomatic Carotid Endarterectomy Trial

TOF:

Time-of-flight

QSM:

Quantitative susceptibility mapping

References

  1. Feigin VL, Forouzanfar MH, Krishnamurthi R, Mensah GA, Connor M, Bennett DA, Moran AE, Sacco RL, Anderson L, Truelsen T, O'Donnell M, Venketasubramanian N, Barker-Collo S, Lawes CM, Wang W, Shinohara Y, Witt E, Ezzati M, Naghavi M, Murray C, Global Burden of Diseases I, Risk Factors S, the GBDSEG (2014) Global and regional burden of stroke during 1990-2010: findings from the Global Burden of Disease Study 2010. Lancet 383(9913):245–254

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bos D, Portegies ML, van der Lugt A, Bos MJ, Koudstaal PJ, Hofman A, Krestin GP, Franco OH, Vernooij MW, Ikram MA (2014) Intracranial carotid artery atherosclerosis and the risk of stroke in whites: the Rotterdam Study. JAMA Neurol 71(4):405–411. doi:10.1001/jamaneurol.2013.6223

    Article  PubMed  Google Scholar 

  3. Xu Y, Yuan C, Zhou Z, He L, Mi D, Li R, Cui Y, Wang Y, Wang Y, Liu G, Zheng Z, Zhao X (2016) Co-existing intracranial and extracranial carotid artery atherosclerotic plaques and recurrent stroke risk: a three-dimensional multicontrast cardiovascular magnetic resonance study. J Cardiovasc Magn Reson 18(1):90. doi:10.1186/s12968-016-0309-3

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bugnicourt JM, Chillon JM, Massy ZA, Canaple S, Lamy C, Deramond H, Godefroy O (2009) High prevalence of intracranial artery calcification in stroke patients with CKD: a retrospective study. Clin J Am Soc Nephrol 4(2):284–290. doi:10.2215/CJN.02140508

    Article  PubMed  PubMed Central  Google Scholar 

  5. Pikija S, Magdic J, Hojs-Fabjan T (2013) Calcifications of vertebrobasilar arteries on CT: detailed distribution and relation to risk factors in 245 ischemic stroke patients. Biomed Res Int 2013:918970. doi:10.1155/2013/918970

    Article  PubMed  PubMed Central  Google Scholar 

  6. Sohn YH, Cheon HY, Jeon P, Kang SY (2004) Clinical implication of cerebral artery calcification on brain CT. Cerebrovasc Dis 18(4):332–337. doi:10.1159/000080772

    Article  PubMed  Google Scholar 

  7. Erbay S, Han R, Baccei S, Krakov W, Zou KH, Bhadelia R, Polak J (2007) Intracranial carotid artery calcification on head CT and its association with ischemic changes on brain MRI in patients presenting with stroke-like symptoms: retrospective analysis. Neuroradiology 49(1):27–33. doi:10.1007/s00234-006-0159-z

    Article  CAS  PubMed  Google Scholar 

  8. Pletcher MJ, Sibley CT, Pignone M, Vittinghoff E, Greenland P (2013) Interpretation of the coronary artery calcium score in combination with conventional cardiovascular risk factors: the multi-ethnic study of atherosclerosis (MESA). Circulation 128(10):1076–1084. doi:10.1161/CIRCULATIONAHA.113.002598

    Article  PubMed  Google Scholar 

  9. Wu XH, Chen XY, Wang LJ, Wong KS (2016) Intracranial artery calcification and its clinical significance. J Clin Neurol 12(3):253–261. doi:10.3988/jcn.2016.12.3.253

    Article  PubMed  PubMed Central  Google Scholar 

  10. Vos A, Van Hecke W, Spliet WG, Goldschmeding R, Isgum I, Kockelkoren R, Bleys RL, Mali WP, de Jong PA, Vink A (2016) Predominance of nonatherosclerotic internal elastic lamina calcification in the intracranial internal carotid artery. Stroke 47(1):221–223. doi:10.1161/STROKEAHA.115.011196

    Article  PubMed  Google Scholar 

  11. Quiney B, Ying SM, Hippe DS, Balu N, Urdaneta-Moncada AR, Mosa-Basha M (2017) The Association of Intracranial Vascular Calcification and Stenosis with Acute Ischemic Cerebrovascular Events. J Comput Assist Tomogr. doi:10.1097/RCT.0000000000000629

  12. Ovesen C, Abild A, Christensen AF, Rosenbaum S, Hansen CK, Havsteen I, Nielsen JK, Christensen H (2013) Prevalence and long-term clinical significance of intracranial atherosclerosis after ischaemic stroke or transient ischaemic attack: a cohort study. BMJ Open 3(10):e003724. doi:10.1136/bmjopen-2013-003724

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kiroglu Y, Calli C, Karabulut N, Oncel C (2010) Intracranial calcifications on CT. Diagn Interv Radiol 16(4):263–269. doi:10.4261/1305-3825.DIR.2626-09.1

    PubMed  Google Scholar 

  14. Chen XY, Lam WW, Ng HK, Fan YH, Wong KS (2007) Intracranial artery calcification: a newly identified risk factor of ischemic stroke. J Neuroimaging 17(4):300–303. doi:10.1111/j.1552-6569.2007.00158.x

    Article  PubMed  Google Scholar 

  15. Mazighi M, Labreuche J, Gongora-Rivera F, Duyckaerts C, Hauw JJ, Amarenco P (2009) Autopsy prevalence of proximal extracranial atherosclerosis in patients with fatal stroke. Stroke 40(3):713–718. doi:10.1161/STROKEAHA.108.514349

    Article  PubMed  Google Scholar 

  16. Moulin T, Tatu L, Vuillier F, Berger E, Chavot D, Rumbach L (2000) Role of a stroke data bank in evaluating cerebral infarction subtypes: patterns and outcome of 1,776 consecutive patients from the Besancon stroke registry. Cerebrovasc dis 10 (4):261-271. Doi:16068

  17. Caplan LR, Wityk RJ, Glass TA, Tapia J, Pazdera L, Chang HM, Teal P, Dashe JF, Chaves CJ, Breen JC, Vemmos K, Amarenco P, Tettenborn B, Leary M, Estol C, Dewitt LD, Pessin MS (2004) New England Medical Center Posterior Circulation registry. Ann Neurol 56(3):389–398. doi:10.1002/ana.20204

    Article  PubMed  Google Scholar 

  18. Chen W, Zhu W, Kovanlikaya I, Kovanlikaya A, Liu T, Wang S, Salustri C, Wang Y (2014) Intracranial calcifications and hemorrhages: characterization with quantitative susceptibility mapping. Radiology 270(2):496–505. doi:10.1148/radiol.13122640

    Article  PubMed  PubMed Central  Google Scholar 

  19. Haacke EM, Mittal S, Wu Z, Neelavalli J, Cheng YC (2009) Susceptibility-weighted imaging: technical aspects and clinical applications, part 1. AJNR Am J Neuroradiol 30(1):19–30. doi:10.3174/ajnr.A1400

    Article  CAS  PubMed  Google Scholar 

  20. Mittal S, Wu Z, Neelavalli J, Haacke EM (2009) Susceptibility-weighted imaging: technical aspects and clinical applications, part 2. AJNR Am J Neuroradiol 30(2):232–252. doi:10.3174/ajnr.A1461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Haacke EM, Xu Y, Cheng YC, Reichenbach JR (2004) Susceptibility weighted imaging (SWI). Magn Reson Med 52(3):612–618. doi:10.1002/mrm.20198

    Article  PubMed  Google Scholar 

  22. Mamlouk MD, Tsai FY, Drachman D, Stradling D, Hasso AN (2012) Cerebral thromboembolism: value of susceptibility-weighted imaging in the initial diagnosis of acute infarction. Neuroradiol J 25(1):45–56

    Article  CAS  PubMed  Google Scholar 

  23. Zhu WZ, Qi JP, Zhan CJ, Shu HG, Zhang L, Wang CY, Xia LM, Hu JW, Feng DY (2008) Magnetic resonance susceptibility weighted imaging in detecting intracranial calcification and hemorrhage. Chin Med J 121(20):2021–2025

    PubMed  Google Scholar 

  24. Kim TW, Choi HS, Koo J, Jung SL, Ahn KJ, Kim BS, Shin YS, Lee KS (2013) Intramural hematoma detection by susceptibility-weighted imaging in intracranial vertebral artery dissection. Cerebrovasc Dis 36(4):292–298. doi:10.1159/000354811

    Article  PubMed  Google Scholar 

  25. Yang Q, Liu J, Barnes SR, Wu Z, Li K, Neelavalli J, Hu J, Haacke EM (2009) Imaging the vessel wall in major peripheral arteries using susceptibility-weighted imaging. J Magn Reson Imaging 30(2):357–365. doi:10.1002/jmri.21859

    Article  PubMed  PubMed Central  Google Scholar 

  26. Barnes SR, Haacke EM (2009) Susceptibility-weighted imaging: clinical angiographic applications. Magn Reson Imaging Clin N Am 17(1):47–61. doi:10.1016/j.mric.2008.12.002

    Article  PubMed  PubMed Central  Google Scholar 

  27. McCollough CH, Ulzheimer S, Halliburton SS, Shanneik K, White RD, Kalender WA (2007) Coronary artery calcium: a multi-institutional, multimanufacturer international standard for quantification at cardiac CT. Radiology 243(2):527–538. doi:10.1148/radiol.2432050808

    Article  PubMed  Google Scholar 

  28. North American Symptomatic Carotid Endarterectomy Trial C, HJM B, Taylor DW, Haynes RB, Sackett DL, Peerless SJ, Ferguson GG, Fox AJ, Rankin RN, Hachinski VC, Wiebers DO, Eliasziw M (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325(7):445–453. doi:10.1056/NEJM199108153250701

    Article  Google Scholar 

  29. Debrey SM, Yu H, Lynch JK, Lovblad KO, Wright VL, Janket SJ, Baird AE (2008) Diagnostic accuracy of magnetic resonance angiography for internal carotid artery disease: a systematic review and meta-analysis. Stroke 39(8):2237–2248. doi:10.1161/STROKEAHA.107.509877

    Article  PubMed  Google Scholar 

  30. Cloud GC, Markus HS (2003) Diagnosis and management of vertebral artery stenosis. QJM 96(1):27–54

    Article  CAS  PubMed  Google Scholar 

  31. Perren F, Poglia D, Landis T, Sztajzel R (2007) Vertebral artery hypoplasia: a predisposing factor for posterior circulation stroke? Neurology 68(1):65–67. doi:10.1212/01.wnl.0000250258.76706.98

    Article  PubMed  Google Scholar 

  32. Mitsumura H, Miyagawa S, Komatsu T, Hirai T, Kono Y, Iguchi Y (2016) Relationship between vertebral artery hypoplasia and posterior circulation ischemia. J Stroke Cerebrovasc Dis 25(2):266–269. doi:10.1016/j.jstrokecerebrovasdis.2015.09.027

    Article  PubMed  Google Scholar 

  33. Khan S, Cloud GC, Kerry S, Markus HS (2007) Imaging of vertebral artery stenosis: a systematic review. J Neurol Neurosurg Psychiatry 78(11):1218–1225. doi:10.1136/jnnp.2006.111716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Muhlenbruch G, Das M, Mommertz G, Schaaf M, Langer S, Mahnken AH, Wildberger JE, Thron A, Gunther RW, Krings T (2010) Comparison of dual-source CT angiography and MR angiography in preoperative evaluation of intra- and extracranial vessels: a pilot study. Eur Radiol 20(2):469–476. doi:10.1007/s00330-009-1547-7

    Article  PubMed  Google Scholar 

  35. Townsend TC, Saloner D, Pan XM, Rapp JH (2003) Contrast material-enhanced MRA overestimates severity of carotid stenosis, compared with 3D time-of-flight MRA. J Vasc Surg 38(1):36–40

    Article  PubMed  Google Scholar 

  36. Li Q, Tian CL, Yang YW, Lou X, Yu SY (2015) Conventional T2-weighted imaging to detect high-grade stenosis and occlusion of internal carotid artery, vertebral artery, and basilar artery. J Stroke Cerebrovasc Dis 24(7):1591–1596. doi:10.1016/j.jstrokecerebrovasdis.2015.03.028

    Article  PubMed  Google Scholar 

  37. Choi CG, Lee DH, Lee JH, Pyun HW, Kang DW, Kwon SU, Kim JK, Kim SJ, Suh DC (2007) Detection of intracranial atherosclerotic steno-occlusive disease with 3D time-of-flight magnetic resonance angiography with sensitivity encoding at 3T. AJNR Am J Neuroradiol 28(3):439–446

    CAS  PubMed  Google Scholar 

  38. Nicoll R, Henein MY (2013) Arterial calcification: friend or foe? Int J Cardiol 167(2):322–327. doi:10.1016/j.ijcard.2012.06.110

    Article  PubMed  Google Scholar 

  39. Liu Q, Fan Z, Yang Q, Li D (2012) Peripheral arterial wall imaging using contrast-enhanced, susceptibility-weighted phase imaging. J Comput Assist Tomogr 36(1):77–82. doi:10.1097/RCT.0b013e3182388cdf

    Article  PubMed  PubMed Central  Google Scholar 

  40. Wu Z, Mittal S, Kish K, Yu Y, Hu J, Haacke EM (2009) Identification of calcification with MRI using susceptibility-weighted imaging: a case study. J Magn Reson Imaging 29(1):177–182. doi:10.1002/jmri.21617

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wang Y, Liu T (2015) Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker. Magn Reson Med 73(1):82–101. doi:10.1002/mrm.25358

    Article  CAS  PubMed  Google Scholar 

  42. Wang R, Xie G, Zhai M, Zhang Z, Wu B, Zheng D, Hong N, Jiang T, Wen B, Cheng J (2017) Stability of R2* and quantitative susceptibility mapping of the brain tissue in a large scale multi-center study. Sci Rep 7:45261. doi:10.1038/srep45261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Gasparotti R, Pinelli L, Liserre R (2011) New MR sequences in daily practice: susceptibility weighted imaging. A pictorial essay. Insights Imaging 2(3):335–347. doi:10.1007/s13244-011-0086-3

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Radiology, Charité, Charitéplatz 1, 10117, Berlin, Germany

    Lisa C. Adams, Sarah M. Böker, Yvonne Y. Bender, Moritz Wagner, Bernd Hamm & Marcus R. Makowski

  2. Department of Radiology, Charité, Augustenburger Platz 1, 13353, Berlin, Germany

    Eva M. Fallenberg

  3. Department of Neuroradiology, Charité, Charitéplatz 1, 10117, Berlin, Germany

    Thomas Liebig

Authors
  1. Lisa C. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah M. Böker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yvonne Y. Bender
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eva M. Fallenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Moritz Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thomas Liebig
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bernd Hamm
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marcus R. Makowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lisa C. Adams.

Ethics declarations

Funding

LCA was supported by the Charité Junior Clinician Scientist program funded by the Charité – Universitaetsmedizin Berlin and the Berlin Institute of Health.

Conflict of interest

MRM has received grants from the Deutsche Forschungsgesellschaft (DFG, 5943/31/41/91) and the GIF (German Israel Research Foundation). BH has received research grants for the Department of Radiology, Charité – Universitätsmedizin Berlin from the following companies: (1) Abbott, (2) Actelion Pharmaceuticals, (3) Bayer Schering Pharma, (4) Bayer Vital, (5) BRACCO Group, (6) Bristol-Myers Squibb, (7) Charite Research Organisation GmbH, (8) Deutsche Krebshilfe, (9) Dt. Stiftung für Herzforschung, (10) Essex Pharma, (11) EU Programmes, (12) Fibrex Medical Inc., (13) Focused Ultrasound Surgery Foundation, (14) Fraunhofer Gesellschaft, (15) Guerbet, (16) INC Research, (17) lnSightec Ud., (18) IPSEN Pharma, (19) Kendlel MorphoSys AG, (20) Lilly GmbH, (21) Lundbeck GmbH, (22) MeVis Medical Solutions AG, (23) Nexus Oncology, (24) Novartis, (25) Parexel Clinical Research Organization Service, (26) Perceptive, (27) Pfizer GmbH, (28) Philipps, (29) Sanofis-Aventis S.A, (30) Siemens, (31) Spectranetics GmbH, (32) Terumo Medical Corporation, (33) TNS Healthcare GMbH, (34) Toshiba, (35) UCB Pharma, (36) Wyeth Pharma, (37) Zukunftsfond Berlin (TSB), (38) Amgen, (39) AO Foundation, (40) BARD, (41) BBraun, (42) Boehring Ingelheimer, (43) Brainsgate, (44) PPD (Clinical Research Organization), (45) CELLACT Pharma, (46) Celgene, (47) CeloNova BioSciences, (48) Covance, (49) DC Deviees, Inc. USA, (50) Ganymed, (51) Gilead Sciences, (52) Glaxo Smith Kline, (53) ICON (Clinical Research Organization), (54) Jansen, (55) LUX Bioseienees, (56) MedPass, (57) Merek, (58) Mologen, (59) Nuvisan, (60) Pluristem, (61) Quintiles, (62) Roehe, (63) Sehumaeher GmbH (Sponsoring eines Workshops), (64) Seattle Geneties, (65) Symphogen, (66) TauRx Therapeuties Ud., (67) Accovion, (68) AIO: Arbeitsgemeinschaft Internistische Onkologie, (69) ASR Advanced sleep research, (70) Astellas, (71) Theradex, (72) Galena Biopharma, (73) Chiltern, (74) PRAint, (75) lnspiremd, (76) Medronic, (77) Respicardia, (78) Silena Therapeutics, (79) Spectrum Pharmaceuticals and (80) St. Jude. The funding had no role in study design, data collection or analysis.

Ethical approval

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. For this type of study formal consent is not required.

Informed consent

For this type of retrospective study formal consent is not required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adams, L.C., Böker, S.M., Bender, Y.Y. et al. Detection of vessel wall calcifications in vertebral arteries using susceptibility weighted imaging. Neuroradiology 59, 861–872 (2017). https://doi.org/10.1007/s00234-017-1878-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-017-1878-z

Keywords

Search

Navigation