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Direct visualization of deep brain stimulation targets in patients with Parkinson’s disease via 3-T quantitative susceptibility mapping

  • Original Article - Functional Neurosurgery - Movement disorders
  • Published:
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Abstract

Background

The direct visualization of brain nuclei on magnetic resonance (MR) images is important for target localization during deep brain stimulation (DBS) in patients with Parkinson’s disease (PD). We demonstrated the superiority of 3-T high-resolution submillimeter voxel size quantitative susceptibility mapping (QSM) for delineating the subthalamic nucleus (STN) and the globus pallidus internus (GPi).

Methods

Preoperative 3-T QSM and T2 weighted (T2w) images were obtained from ten patients with PD. Qualitative visualization scores were analyzed by two neurosurgeons on both images using a 4-point and 5-point scale, respectively. Images were also compared with regard to contrast-to-noise ratios (CNRs) and edge detection power for the STN and GPi. The Wilcoxon rank-sum test and the signed-rank test were used to compare measurements between the two images.

Results

Visualization scores for the STN and GPi, the mean CNR of the STN relative to the zona incerta (ZI) and the substantia nigra, and the mean CNR of the GPi relative to the internal capsule (IC) and the globus pallidum externum, were significantly higher on QSM images than on T2w images (P < 0.01). The edge detection powers of the STN-ZI and GPi-IC on QSM were significantly larger (by 2.6- and 3.8-fold, respectively) than those on T2w images (P < 0.01). QSM detected asymmetry of the STN in two patients.

Conclusions

QSM images provided improved delineation ability for the STN and GPi when compared to T2w images. Our findings are important for patients with PD who undergo DBS surgery, particularly those with asymmetric bilateral nuclei.

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Abbreviations

PD:

Parkinson’s disease

DBS:

deep brain stimulation

STN:

subthalamic nucleus

GPi:

globus pallidus interna

ZI:

zona incerta

SN:

substantia nigra

IC:

internal capsule

GPe:

globus pallidum externum

T2w:

T2-weighted

QSM:

quantitative susceptibility mapping

GRE:

gradient recalled echo

MIL:

medial intermedullary lamina

CNR:

contrast-to-noise ratio

ROI:

regions of interest

SD:

standard deviation

MER:

microelectrode recordings

References

  1. Abosch A, Yacoub E, Ugurbil K, Harel N (2010) An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery 67:1745–1756; discussion 1756. https://doi.org/10.1227/NEU.0b013e3181f74105

    Article  PubMed  PubMed Central  Google Scholar 

  2. Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266–271. https://doi.org/10.1016/0166-2236(90)90107-l

    Article  CAS  PubMed  Google Scholar 

  3. Andrade-Souza YM, Schwalb JM, Hamani C, Eltahawy H, Hoque T, Saint-Cyr J, Lozano AM (2008) Comparison of three methods of targeting the subthalamic nucleus for chronic stimulation in Parkinson's disease. Neurosurgery 62(Suppl 2):875–883. https://doi.org/10.1227/01.neu.0000316289.75736.55

    Article  PubMed  Google Scholar 

  4. Ashkan K, Blomstedt P, Zrinzo L, Tisch S, Yousry T, Limousin-Dowsey P, Hariz MI (2007) Variability of the subthalamic nucleus: the case for direct MRI guided targeting. Br J Neurosurg 21:197–200. https://doi.org/10.1080/02688690701272240

    Article  CAS  PubMed  Google Scholar 

  5. Brass SD, Chen NK, Mulkern RV, Bakshi R (2006) Magnetic resonance imaging of iron deposition in neurological disorders. Top Magn Reson Imaging 17:31–40. https://doi.org/10.1097/01.rmr.0000245459.82782.e4

    Article  PubMed  Google Scholar 

  6. Bronstein JM, Tagliati M, Alterman RL, Lozano AM, Volkmann J, Stefani A, Horak FB, Okun MS, Foote KD, Krack P, Pahwa R, Henderson JM, Hariz MI, Bakay RA, Rezai A, Marks WJ Jr, Moro E, Vitek JL, Weaver FM, Gross RE, DeLong MR (2011) Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol 68:165. https://doi.org/10.1001/archneurol.2010.260

    Article  PubMed  Google Scholar 

  7. Chandran AS, Bynevelt M, Lind CR (2016) Magnetic resonance imaging of the subthalamic nucleus for deep brain stimulation. J Neurosurg 124:96–105. https://doi.org/10.3171/2015.1.JNS142066

    Article  PubMed  Google Scholar 

  8. Cho ZH, Min HK, Oh SH, Han JY, Park CW, Chi JG, Kim YB, Paek SH, Lozano AM, Lee KH (2010) Direct visualization of deep brain stimulation targets in Parkinson disease with the use of 7-tesla magnetic resonance imaging. J Neurosurg 113:639–647. https://doi.org/10.3171/2010.3.JNS091385

    Article  PubMed  PubMed Central  Google Scholar 

  9. Cif L, Hariz M (2017) Seventy years with the Globus Pallidus: Pallidal surgery for movement disorders between 1947 and 2017. Mov Disord 32:972–982. https://doi.org/10.1002/mds.27054

    Article  PubMed  Google Scholar 

  10. Cuny E, Guehl D, Burbaud P, Gross C, Dousset V, Rougier A (2002) Lack of agreement between direct magnetic resonance imaging and statistical determination of a subthalamic target: the role of electrophysiological guidance. J Neurosurg 97:591–597. https://doi.org/10.3171/jns.2002.97.3.0591

    Article  PubMed  Google Scholar 

  11. Curot J, Valton L, Denuelle M, Vignal JP, Maillard L, Pariente J, Trebuchon A, Bartolomei F, Barbeau EJ (2018) Deja-reve: prior dreams induced by direct electrical brain stimulation. Brain Stimul 11:875–885. https://doi.org/10.1016/j.brs.2018.02.016

    Article  PubMed  PubMed Central  Google Scholar 

  12. Dimov A, Patel W, Yao Y, Wang Y, O'Halloran R, Kopell BH (2019) Iron concentration linked to structural connectivity in the subthalamic nucleus: implications for deep brain stimulation. J Neurosurg:1–8. https://doi.org/10.3171/2018.8.JNS18531

  13. Dimov AV, Gupta A, Kopell BH, Wang Y (2018) High-resolution QSM for functional and structural depiction of subthalamic nuclei in DBS presurgical mapping. J Neurosurg 131:360–367. https://doi.org/10.3171/2018.3.JNS172145

    Article  PubMed  Google Scholar 

  14. Dormont D, Ricciardi KG, Tande D, Parain K, Menuel C, Galanaud D, Navarro S, Cornu P, Agid Y, Yelnik J (2004) Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. AJNR Am J Neuroradiol 25:1516–1523

    PubMed  Google Scholar 

  15. Gross RE, Krack P, Rodriguez-Oroz MC, Rezai AR, Benabid AL (2006) Electrophysiological mapping for the implantation of deep brain stimulators for Parkinson's disease and tremor. Mov Disord 21(Suppl 14):S259–S283. https://doi.org/10.1002/mds.20960

    Article  PubMed  Google Scholar 

  16. Guehl D, Cuny E, Benazzouz A, Rougier A, Tison F, Machado S, Grabot D, Gross C, Bioulac B, Burbaud P (2006) Side-effects of subthalamic stimulation in Parkinson's disease: clinical evolution and predictive factors. Eur J Neurol 13:963–971. https://doi.org/10.1111/j.1468-1331.2006.01405.x

    Article  CAS  PubMed  Google Scholar 

  17. Guridi J, Rodriguez-Oroz MC, Lozano AM, Moro E, Albanese A, Nuttin B, Gybels J, Ramos E, Obeso JA (2000) Targeting the basal ganglia for deep brain stimulation in Parkinson's disease. Neurology 55:S21–S28

    Article  CAS  Google Scholar 

  18. Hamani C, Richter EO, Andrade-Souza Y, Hutchison W, Saint-Cyr JA, Lozano AM (2005) Correspondence of microelectrode mapping with magnetic resonance imaging for subthalamic nucleus procedures. Surg Neurol 63:249–253; discussion 253. https://doi.org/10.1016/j.surneu.2004.05.036

    Article  PubMed  Google Scholar 

  19. Hariz MI, Krack P, Melvill R, Jorgensen JV, Hamel W, Hirabayashi H, Lenders M, Wesslen N, Tengvar M, Yousry TA (2003) A quick and universal method for stereotactic visualization of the subthalamic nucleus before and after implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg 80:96–101. https://doi.org/10.1159/000075167

    Article  PubMed  Google Scholar 

  20. Hirabayashi H, Hariz MI, Fagerlund M (1998) Comparison between stereotactic CT and MRI coordinates of pallidal and thalamic targets using the Laitinen noninvasive stereoadapter. Stereotact Funct Neurosurg 71:117–130. https://doi.org/10.1159/000029655

    Article  CAS  PubMed  Google Scholar 

  21. Hirabayashi H, Tengvar M, Hariz MI (2002) Stereotactic imaging of the pallidal target. Mov Disord 17(Suppl 3):S130–S134. https://doi.org/10.1002/mds.10154

    Article  PubMed  Google Scholar 

  22. Hyam JA, Akram H, Foltynie T, Limousin P, Hariz M, Zrinzo L (2015) What you see is what you get: Lead location within deep brain structures is accurately depicted by stereotactic magnetic resonance imaging. Neurosurgery 11(Suppl 3):412–419; discussion 419. https://doi.org/10.1227/NEU.0000000000000848

    Article  PubMed  Google Scholar 

  23. Just M, Thelen M (1988) Tissue characterization with T1, T2, and proton density values: results in 160 patients with brain tumors. Radiology 169:779–785. https://doi.org/10.1148/radiology.169.3.3187000

    Article  CAS  PubMed  Google Scholar 

  24. Langkammer C, Schweser F, Krebs N, Deistung A, Goessler W, Scheurer E, Sommer K, Reishofer G, Yen K, Fazekas F, Ropele S, Reichenbach JR (2012) Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage 62:1593–1599. https://doi.org/10.1016/j.neuroimage.2012.05.049

    Article  PubMed  PubMed Central  Google Scholar 

  25. Liu T, Eskreis-Winkler S, Schweitzer AD, Chen W, Kaplitt MG, Tsiouris AJ, Wang Y (2013) Improved subthalamic nucleus depiction with quantitative susceptibility mapping. Radiology 269:216–223. https://doi.org/10.1148/radiol.13121991

    Article  PubMed  PubMed Central  Google Scholar 

  26. Mai JK (2016) Atlas of the human brain. 4th Ed.

  27. Massey LA, Miranda MA, Zrinzo L, Al-Helli O, Parkes HG, Thornton JS, So PW, White MJ, Mancini L, Strand C, Holton JL, Hariz MI, Lees AJ, Revesz T, Yousry TA (2012) High resolution MR anatomy of the subthalamic nucleus: imaging at 9.4 T with histological validation. Neuroimage 59:2035–2044. https://doi.org/10.1016/j.neuroimage.2011.10.016

    Article  CAS  PubMed  Google Scholar 

  28. McIntyre CC, Mori S, Sherman DL, Thakor NV, Vitek JL (2004) Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus. Clin Neurophysiol 115:589–595. https://doi.org/10.1016/j.clinph.2003.10.033

    Article  PubMed  Google Scholar 

  29. O'Gorman RL, Jarosz JM, Samuel M, Clough C, Selway RP, Ashkan K (2009) CT/MR image fusion in the postoperative assessment of electrodes implanted for deep brain stimulation. Stereotact Funct Neurosurg 87:205–210. https://doi.org/10.1159/000225973

    Article  PubMed  Google Scholar 

  30. O'Gorman RL, Shmueli K, Ashkan K, Samuel M, Lythgoe DJ, Shahidiani A, Wastling SJ, Footman M, Selway RP, Jarosz J (2011) Optimal MRI methods for direct stereotactic targeting of the subthalamic nucleus and globus pallidus. Eur Radiol 21:130–136. https://doi.org/10.1007/s00330-010-1885-5

    Article  PubMed  Google Scholar 

  31. Patriat R, Cooper SE, Duchin Y, Niederer J, Lenglet C, Aman J, Park MC, Vitek JL, Harel N (2018) Individualized tractography-based parcellation of the globus pallidus pars interna using 7T MRI in movement disorder patients prior to DBS surgery. Neuroimage 178:198–209. https://doi.org/10.1016/j.neuroimage.2018.05.048

    Article  PubMed  PubMed Central  Google Scholar 

  32. Polanski WH, Martin KD, Engellandt K, von Kummer R, Klingelhoefer L, Fauser M, Storch A, Schackert G, Sobottka SB (2015) Accuracy of subthalamic nucleus targeting by T2, FLAIR and SWI-3-tesla MRI confirmed by microelectrode recordings. Acta Neurochir 157:479–486. https://doi.org/10.1007/s00701-014-2328-x

    Article  PubMed  Google Scholar 

  33. Rasouli J, Ramdhani R, Panov FE, Dimov A, Zhang Y, Cho C, Wang Y, Kopell BH (2018) Utilization of quantitative susceptibility mapping for direct targeting of the subthalamic nucleus during deep brain stimulation surgery. Oper Neurosurg (Hagerstown) 14:412–419. https://doi.org/10.1093/ons/opx131

    Article  Google Scholar 

  34. Schafer A, Forstmann BU, Neumann J, Wharton S, Mietke A, Bowtell R, Turner R (2012) Direct visualization of the subthalamic nucleus and its iron distribution using high-resolution susceptibility mapping. Hum Brain Mapp 33:2831–2842. https://doi.org/10.1002/hbm.21404

    Article  PubMed  Google Scholar 

  35. Shamir RR, Duchin Y, Kim J, Patriat R, Marmor O, Bergman H, Vitek JL, Sapiro G, Bick A, Eliahou R, Eitan R, Israel Z, Harel N (2019) Microelectrode recordings validate the clinical visualization of subthalamic-nucleus based on 7T magnetic resonance imaging and machine learning for deep brain stimulation surgery. Neurosurgery 84:749–757. https://doi.org/10.1093/neuros/nyy212

    Article  PubMed  Google Scholar 

  36. Skogseid IM (2008) Pallidal deep brain stimulation is effective, and improves quality of life in primary segmental and generalized dystonia. Acta Neurol Scand Suppl 188:51–55. https://doi.org/10.1111/j.1600-0404.2008.01032.x

    Article  CAS  PubMed  Google Scholar 

  37. Starr PA, Christine CW, Theodosopoulos PV, Lindsey N, Byrd D, Mosley A, Marks WJ Jr (2002) Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg 97:370–387. https://doi.org/10.3171/jns.2002.97.2.0370

    Article  PubMed  Google Scholar 

  38. Sumanaweera TS, Adler JR Jr, Napel S, Glover GH (1994) Characterization of spatial distortion in magnetic resonance imaging and its implications for stereotactic surgery. Neurosurgery 35:696–703; discussion 703-694. https://doi.org/10.1227/00006123-199410000-00016

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  40. Wei H, Dibb R, Zhou Y, Sun Y, Xu J, Wang N, Liu C (2015) Streaking artifact reduction for quantitative susceptibility mapping of sources with large dynamic range. NMR Biomed 28:1294–1303. https://doi.org/10.1002/nbm.3383

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wei H, Zhang C, Wang T, He N, Li D, Zhang Y, Liu C, Yan F, Sun B (2019) Precise targeting of the globus pallidus internus with quantitative susceptibility mapping for deep brain stimulation surgery. J Neurosurg:1–7. https://doi.org/10.3171/2019.7.JNS191254

  42. Wei H, Zhang Y, Gibbs E, Chen NK, Wang N, Liu C (2017) Joint 2D and 3D phase processing for quantitative susceptibility mapping: application to 2D echo-planar imaging. NMR Biomed 30. https://doi.org/10.1002/nbm.3501

  43. Zabek M, Sobstyl M, Koziara H, Kadziolka B, Mossakowski Z, Dzierzecki S (2010) Bilateral subthalamic nucleus stimulation in the treatment of advanced Parkinson's disease. Five years' personal experience. Neurol Neurochir Pol 44:3–12

    Article  Google Scholar 

  44. Zonenshayn M, Rezai AR, Mogilner AY, Beric A, Sterio D, Kelly PJ (2000) Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. Neurosurgery 47:282–292; discussion 292-284. https://doi.org/10.1097/00006123-200008000-00005

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

KY, ZR, and SG collected and analyzed the data. KY drafted the manuscript. ZR, JL, and YH helped to modify the manuscript. YL contributed to the conception and the design. All authors read and approved the manuscript.

Funding

Beijing Municipal Science & Technology Commission provided financial support (Reference: Z181100001718056). The sponsor had no role in the design or conduct of this research.

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Correspondence to Yongjie Li.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (name of institute/committee) and complied with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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A nice technical study showing that 3 Tesla high-resolution quantitative susceptibility mapping MRI has potential beneficial qualitative and quantitative proporties of depicting the STN and GPi for direct targeting in DBS surgeries compared to conventional T2 MRI.

Felix Gubler

Maastricht, Netherlands

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This article is part of the Topical Collection on Functional Neurosurgery - Movement disorders

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Yu, K., Ren, Z., Li, J. et al. Direct visualization of deep brain stimulation targets in patients with Parkinson’s disease via 3-T quantitative susceptibility mapping. Acta Neurochir 163, 1335–1345 (2021). https://doi.org/10.1007/s00701-021-04715-4

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