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Quantitative Susceptibility Mapping of the Substantia Nigra in Parkinson’s Disease

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Abstract

The purpose of this study was to evaluate the sensitivities of quantitative susceptibility mapping (QSM) and R2* mapping in clinical diagnoses of Parkinson’s disease (PD). QSM images and R2* maps from 29 patients with PD and 25 healthy controls were obtained on a clinical 3T magnetic resonance imaging (MRI) system using a three-dimensional multi-echo gradient-echo sequence. Two-tailed t tests and receiver operating characteristic curves analyses were applied to the mean values of QSM and R2* of the two groups. In the PD group, a two-tailed Pearson correlation analysis was used to investigate the correlations between MRI measures (susceptibility and R2* values) and the Unified Parkinson’s Disease Rating Scale-III (UPDRS-III) score. In the substantia nigra (SN), a significant difference between patients with PD and healthy controls was found on QSM (154.80 ± 43.36 vs. 127.50 ± 21.05 ppb, P = 0.006) but not on R2* mapping. The receiver operating characteristic curves showed that QSM was more sensitive than R2* mapping to distinguish PD patients from healthy controls, with areas under the curve equal to 0.68 and 0.51, respectively. The UPDRS-III motor scores did not correlate with mean susceptibility or R2* values in the PD group. In conclusion, QSM is a more accurate and sensitive method than R2* mapping to detect the pathologic changes in the SN of patients with PD.

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References

  1. P. Damier, E.C. Hirsch, Y. Agid, A.M. Graybiel, Brain 122(Pt 8), 1437–1448 (1999)

    Article  Google Scholar 

  2. K. Seppi, W. Poewe, Neuroimaging Clin. N. Am. 20, 29–55 (2010)

    Article  Google Scholar 

  3. S. Baudrexel, L. Nurnberger, U. Rub, C. Seifried, J.C. Klein, T. Deller, H. Steinmetz, R. Deichmann, R. Hilker, Neuroimage 51, 512–520 (2010)

    Article  Google Scholar 

  4. R.A. Menke, J. Scholz, K.L. Miller, S. Deoni, S. Jbabdi, P.M. Matthews, M. Zarei, Neuroimage 47, 435–441 (2009)

    Article  Google Scholar 

  5. J. Vymazal, A. Righini, R.A. Brooks, M. Canesi, C. Mariani, M. Leonardi, G. Pezzoli, Radiology 211, 489–495 (1999)

    Article  Google Scholar 

  6. D. Aquino, V. Contarino, A. Albanese, L. Minati, L. Farina, M. Grisoli, L. Romita, A.E. Elia, M.G. Bruzzone, L. Chiapparini, Neuroscience 35, 753–758 (2014)

    Google Scholar 

  7. M. Gerlach, K.L. Double, M.B. Youdim, P. Riederer, J. Neural Transm. Suppl. 70, 133–142 (2006)

    Article  Google Scholar 

  8. Z. Lv, H. Jiang, H. Xu, N. Song, J. Xie, J. Neural. Transm. 118, 361–369 (2011)

    Article  Google Scholar 

  9. L. Zecca, A. Stroppolo, A. Gatti, D. Tampellini, M. Toscani, M. Gallorini, G. Giaveri, P. Arosio, P. Santambrogio, R.G. Fariello, E. Karatekin, M.H. Kleinman, N. Turro, O. Hornykiewicz, F.A. Zucca, Proc. Natl. Acad. Sci. USA 101, 9843–9848 (2004)

    Article  ADS  Google Scholar 

  10. P. Peran, A. Cherubini, F. Assogna, F. Piras, C. Quattrocchi, A. Peppe, P. Celsis, O. Rascol, J.F. Demonet, A. Stefani, M. Pierantozzi, F.E. Pontieri, C. Caltagirone, G. Spalletta, U. Sabatini, Brain 133, 3423–3433 (2010)

    Article  Google Scholar 

  11. I. Nestrasil, S. Michaeli, T. Liimatainen, C.E. Rydeen, C.M. Kotz, J.P. Nixon, T. Hanson, P.J. Tuite, J. Neurol. 257, 964–968 (2010)

    Article  Google Scholar 

  12. E.M. Haacke, Y. Miao, M. Liu, C.A. Habib, Y. Katkuri, T. Liu, Z. Yang, Z. Lang, J. Hu, J. Wu, J. Magn. Reson. Imaging 32, 561–576 (2010)

    Article  Google Scholar 

  13. J.M. Graham, M.N. Paley, R.A. Grunewald, N. Hoggard, P.D. Griffiths, Brain 123(Pt 12), 2423–2431 (2000)

    Article  Google Scholar 

  14. B.H. Braffman, R.I. Grossman, H.I. Goldberg, M.B. Stern, H.I. Hurtig, D.B. Hackney, L.T. Bilaniuk, R.A. Zimmerman, A.J.R. Am, J. Roentgenol. 152, 159–165 (1989)

    Article  Google Scholar 

  15. F. Mondino, P. Filippi, U. Magliola, S. Duca, Neurol. Sci. 23(Suppl 2), S87–S88 (2002)

    Article  Google Scholar 

  16. A.J. Walsh, A.H. Wilman, Neuroimage 57, 452–461 (2011)

    Article  Google Scholar 

  17. W. Li, B. Wu, C. Liu, Neuroimage 55, 1645–1656 (2011)

    Article  Google Scholar 

  18. L. de Rochefort, T. Liu, B. Kressler, J. Liu, P. Spincemaille, V. Lebon, J. Wu, Y. Wang, Magn. Reson. Med. 63, 194–206 (2010)

    Google Scholar 

  19. Y. Wang, T. Liu, Magn. Reson. Med. 73, 82–101 (2015)

    Article  Google Scholar 

  20. T. Liu, W. Xu, P. Spincemaille, A.S. Avestimehr, Y. Wang, I.E.E.E. Trans. Med. Imaging 31, 816–824 (2012)

    Article  Google Scholar 

  21. E.M. Haacke, S. Liu, S. Buch, W. Zheng, D. Wu, Y. Ye, Magn. Reson. Imaging 33, 1–25 (2015)

    Article  Google Scholar 

  22. C. Liu, W. Li, K.A. Tong, K.W. Yeom, S. Kuzminski, J. Magn. Reson. Imaging 42, 23–41 (2015)

    Article  Google Scholar 

  23. C. Langkammer, F. Schweser, N. Krebs, A. Deistung, W. Goessler, E. Scheurer, K. Sommer, G. Reishofer, K. Yen, F. Fazekas, S. Ropele, J.R. Reichenbach, Neuroimage 62, 1593–1599 (2012)

    Article  Google Scholar 

  24. J. Li, S. Chang, T. Liu, Q. Wang, D. Cui, X. Chen, M. Jin, B. Wang, M. Pei, C. Wisnieff, P. Spincemaille, M. Zhang, Y. Wang, Magn. Reson. Med. 68, 1563–1569 (2012)

    Article  Google Scholar 

  25. Y. Murakami, S. Kakeda, K. Watanabe, I. Ueda, A. Ogasawara, J. Moriya, S. Ide, K. Futatsuya, T. Sato, K. Okada, T. Uozumi, S. Tsuji, T. Liu, Y. Wang, Y. Korogi, Am. J. Neuroradiol. 36, 1102–1108 (2015)

    Article  Google Scholar 

  26. A.K. Lotfipour, S. Wharton, S.T. Schwarz, V. Gontu, A. Schafer, A.M. Peters, R.W. Bowtell, D.P. Auer, P.A. Gowland, N.P. Bajaj, J. Magn. Reson. Imaging 35, 48–55 (2012)

    Article  Google Scholar 

  27. J.H. Barbosa, A.C. Santos, V. Tumas, M. Liu, W. Zheng, E.M. Haacke, C.E. Salmon, Magn. Reson. Imaging 33, 559–565 (2015)

    Article  Google Scholar 

  28. A. Ojelade, T. Jia, A.R. Rodan, T. Chenyang, J.L. Kadrmas, A. Cattrell, B. Ruggeri, P. Charoen, H. Lemaitre, T. Banaschewski, C. Buchel, A.L. Bokde, F. Carvalho, P.J. Conrod, H. Flor, V. Frouin, J. Gallinat, H. Garavan, P.A. Gowland, A. Heinz, B. Ittermann, M. Lathrop, S. Lubbe, J.L. Martinot, T. Paus, M.N. Smolka, R. Spanagel, P.F. O’Reilly, J. Laitinen, J.M. Veijola, J. Feng, S. Desrivieres, M.R. Jarvelin, I. Consortium, G. Schumann, A. Rothenfluh, Proc. Natl. Acad. Sci. USA 112, E4085–E4093 (2015)

    Article  Google Scholar 

  29. G. Du, T. Liu, M.M. Lewis, L. Kong, Y. Wang, J. Connor, R.B. Mailman, X. Huang, Mov. Disord. 31(3), 317–324 (2016)

    Article  Google Scholar 

  30. J. Liu, T. Liu, L. de Rochefort, J. Ledoux, I. Khalidov, W. Chen, A.J. Tsiouris, C. Wisnieff, P. Spincemaille, M.R. Prince, Y. Wang, Neuroimage 59, 2560–2568 (2012)

    Article  Google Scholar 

  31. T. Liu, C. Wisnieff, M. Lou, W. Chen, P. Spincemaille, Y. Wang, Magn. Reson. Med. 69, 467–476 (2013)

    Article  Google Scholar 

  32. R. Cusack, N. Papadakis, Neuroimage 16, 754–764 (2002)

    Article  Google Scholar 

  33. T. Liu, I. Khalidov, L. de Rochefort, P. Spincemaille, J. Liu, A.J. Tsiouris, Y. Wang, NMR Biomed. 24, 1129–1136 (2011)

    Article  Google Scholar 

  34. W. Chen, S.A. Gauthier, A. Gupta, J. Comunale, T. Liu, S. Wang, M. Pei, D. Pitt, Y. Wang, Radiology 271, 183–192 (2014)

    Article  Google Scholar 

  35. W. Chen, W. Zhu, I. Kovanlikaya, A. Kovanlikaya, T. Liu, S. Wang, C. Salustri, Y. Wang, Radiology 270, 496–505 (2014)

    Article  Google Scholar 

  36. C. Wisnieff, S. Ramanan, J. Olesik, S. Gauthier, Y. Wang, D. Pitt, Magn. Reson. Med. 74, 564–570 (2015)

    Article  Google Scholar 

  37. B. Xu, T. Liu, P. Spincemaille, M. Prince, Y. Wang, Magn. Reson. Med. 72, 438–445 (2014)

    Article  Google Scholar 

  38. A. Groger, D. Berg, J. Neural. Transm. 119, 1523–1528 (2012)

    Article  Google Scholar 

  39. A. Schafer, B.U. Forstmann, J. Neumann, S. Wharton, A. Mietke, R. Bowtell, R. Turner, Hum. Brain Mapp. 33, 2831–2842 (2012)

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported in part by grants from The National Natural Science Foundation of China (81271533) and Shanghai Municipal Commission of Health and Family Planning (201540392). We thank Kelly Gillen for English editing.

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Author notes

  1. Xinxin Zhao and Hedi An contributed equally to this work (shared first authorship).

Authors and Affiliations

  1. Shanghai Key Laboratory of Magnetic Resonance, Department of Physics, East China Normal University, 3663 North Zhongshan Road, Shanghai, 200062, China

    Xinxin Zhao, Binshi Bo, Zhuwei Zhang, Pengfei Weng, Meining Chen, Mengchao Pei, Yi Wang & Jianqi Li

  2. Department of Neurology, School of Medicine, East Hospital Affiliated to Tongji University, 150 Jimo Road, Pudong, Shanghai, 200120, China

    Hedi An, Nan Shen & Dongya Huang

  3. Department of Radiology, Weill Medical College of Cornell University, 515 East 71st St., Suite S106, New York, NY, 10021, USA

    Tian Liu & Yi Wang

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  1. Xinxin Zhao
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Correspondence to Dongya Huang or Jianqi Li.

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Zhao, X., An, H., Liu, T. et al. Quantitative Susceptibility Mapping of the Substantia Nigra in Parkinson’s Disease. Appl Magn Reson 48, 533–544 (2017). https://doi.org/10.1007/s00723-017-0877-x

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  • DOI: https://doi.org/10.1007/s00723-017-0877-x

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