Skip to main content
SpringerLink
Log in

Quantitative susceptibility mapping in patients with systemic lupus erythematosus: detection of abnormalities in normal-appearing basal ganglia

  • Neuro
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To evaluate whether quantitative susceptibility mapping (QSM) can be employed to detect abnormalities within normal-appearing basal ganglia on conventional MRI in patients with neuropsychiatric systemic lupus erythematosus (NPSLE).

Methods

For 33 SLE patients (13 NPSLE and 20 non-NPSLE patients) and 23 age/sex-matched controls, two radiologists independently measured the mean QSM and R2* values in various brain structures that appeared to be normal on conventional MR images. These values in each brain structure were compared among the two SLE groups and controls.

Results

Regarding the putamen, the NPSLE patients showed significantly higher QSM values than the non-NPSLE patients and controls (p < 0.05). For the lateral globus pallidus, both SLE groups showed significantly higher QSM values than the controls (p < 0.05). The R2* values were not significantly different between both SLE groups. The NPSLE patients showed a significant correlation between the mean QSM values in putamen and the disease duration (r = 0.63, p < 0.05). For the interobserver agreement, the QSM value was superior to the R2* value (0.690 vs. 0.446, Kendall W value).

Conclusions

QSM can be used to identify increased susceptibility of the basal ganglia appearing to be normal on conventional MR images in NPSLE patients.

Key Points

• QSM values in the putamen are significantly higher in NPSLE than non-NPSLE.

• NPSLE patients show correlation between QSM values in the putamen and disease duration.

• QSM is more sensitive than R2* mapping for detecting subtle changes.

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

Similar content being viewed by others

Abbreviations

NPSLE:

Neuropsychiatric systemic lupus erythematosus

SLE:

Systemic lupus erythematosus

QSM:

Quantitative susceptibility mapping

References

  1. O’Connor JF, Musher DM (1966) Central nervous system involvement in systemic lupus erythematosus: a study of 150 cases. Arch Neurol 14:157–164

    Article  PubMed  Google Scholar 

  2. Sibbitt WL Jr, Brooks WM, Kornfeld M, Hart BL, Bankhurst AD, Roldan CA (2010) Magnetic resonance imaging and brain histopathology in neuropsychiatric systemic lupus erythematosus. Semin Arthritis Rheum 40:32–52

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kim JH, Choi C-G, Choi S-J, Lee HK, Suh DC (2000) Primary antiphospholipid antibody syndrome: neuroradiologic findings in 11 patients. Korean J Radiol 1:5–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Golstein M, Meyer O, Bourgeois P et al (1992) Neurological manifestations of systemic lupus erythematosus: role of antiphospholipid antibodies. Clin Exp Rheumatol 11:373–379

    Google Scholar 

  5. Zivadinov R, Shucard J, Hussein S et al (2013) Multimodal imaging in systemic lupus erythematosus patients with diffuse neuropsychiatric involvement. Lupus 22:675–683

    Article  CAS  PubMed  Google Scholar 

  6. Lee S, Park MC, Lee S, Park Y (2012) The efficacy of brain F-fluorodeoxyglucose positron emission tomography in neuropsychiatric lupus patients with normal brain magnetic resonance imaging findings. Lupus 21:1531–1537

    Article  PubMed  Google Scholar 

  7. Zhang X, Zhu Z, Zhang F, Shu H, Li F, Dong Y (2005) Diagnostic value of single-photon-emission computed tomography in severe central nervous system involvement of systemic lupus erythematosus: a case-control study. Arthritis Rheum 53:845–849

    Article  PubMed  Google Scholar 

  8. Popescu A, Kao AH (2011) Neuropsychiatric systemic lupus erythematosus. Curr Neuropharmacol 9:449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Mehta V, Pei W, Yang G et al (2013) Iron is a sensitive biomarker for inflammation in multiple sclerosis lesions. PLoS One 8, e57573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Hametner S, Wimmer I, Haider L, Pfeifenbring S, Brück W, Lassmann H (2013) Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 74:848–861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bagnato F, Hametner S, Yao B et al (2011) Tracking iron in multiple sclerosis: a combined imaging and histopathological study at 7 Tesla. Brain 134:3599–3612

    Article  PubMed Central  Google Scholar 

  12. Langkammer C, Liu T, Khalil M et al (2013) Quantitative susceptibility mapping in multiple sclerosis. Radiology 267:551–559

    Article  PubMed  PubMed Central  Google Scholar 

  13. Walsh AJ, Lebel RM, Eissa A et al (2013) Multiple sclerosis: validation of MR imaging for quantification and detection of iron. Radiology 267:531–542

    Article  PubMed  Google Scholar 

  14. Chen W, Gauthier SA, Gupta A et al (2014) Quantitative susceptibility mapping of multiple sclerosis lesions at various ages. Radiology 271:183–192

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kell DB (2010) Towards a unifying, systems biology understanding of large-scale cellular death and destruction caused by poorly liganded iron: Parkinson’s, Huntington’s, Alzheimer’s, prions, bactericides, chemical toxicology and others as examples. Arch Toxicol 84:825–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Haacke EM, Cheng NY, House MJ et al (2005) Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging 23:1–25

    Article  CAS  PubMed  Google Scholar 

  17. Péran P, Cherubini A, Assogna F et al (2010) Magnetic resonance imaging markers of Parkinson’s disease nigrostriatal signature. Brain 133:3423–3433

    Article  PubMed  Google Scholar 

  18. Yao B, Li T-Q, Pv G, Shmueli K, de Zwart JA, Duyn JH (2009) Susceptibility contrast in high field MRI of human brain as a function of tissue iron content. Neuroimage 44:1259–1266

    Article  PubMed  PubMed Central  Google Scholar 

  19. Wang S, Lou M, Liu T, Cui D, Chen X, Wang Y (2013) Hematoma volume measurement in gradient echo MRI using quantitative susceptibility mapping. Stroke 44:2315–2317

    Article  PubMed  PubMed Central  Google Scholar 

  20. Yablonskiy DA, Haacke EM (1994) Theory of NMR signal behavior in magnetically inhomogeneous tissues: the static dephasing regime. Magn Reson Med 32:749–763

    Article  CAS  PubMed  Google Scholar 

  21. de Rochefort L, Liu T, Kressler B et al (2010) Quantitative susceptibility map reconstruction from MR phase data using bayesian regularization: validation and application to brain imaging. Magn Reson Med 63:194–206

    PubMed  Google Scholar 

  22. Liu T, Wisnieff C, Lou M, Chen W, Spincemaille P, Wang Y (2013) Nonlinear formulation of the magnetic field to source relationship for robust quantitative susceptibility mapping. Magn Reson Med 69:467–476

    Article  PubMed  Google Scholar 

  23. Liu J, Liu T, de Rochefort L et al (2012) Morphology enabled dipole inversion for quantitative susceptibility mapping using structural consistency between the magnitude image and the susceptibility map. Neuroimage 59:2560–2568

    Article  PubMed  PubMed Central  Google Scholar 

  24. Bilgic B, Pfefferbaum A, Rohlfing T, Sullivan EV, Adalsteinsson E (2012) MRI estimates of brain iron concentration in normal aging using quantitative susceptibility mapping. Neuroimage 59:2625–2635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ide S, Kakeda S, Ueda I et al (2014) Internal structures of the globus pallidus in patients with Parkinson’s disease: evaluation with quantitative susceptibility mapping (QSM). Eur Radiol 25:1–9

    Google Scholar 

  26. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725–1725

    Article  CAS  PubMed  Google Scholar 

  27. Ainiala H, Hietaharju A, Loukkola J et al (2001) Validity of the new American College of Rheumatology criteria for neuropsychiatric lupus syndromes: a population-based evaluation. Arthritis Rheum 45:419–423

    Article  CAS  PubMed  Google Scholar 

  28. West SG, Emlen W, Wener MH, Kotzin BL (1995) Neuropsychiatric lupus erythematosus: a 10-year prospective study on the value of diagnostic tests. Am J Med 99:153–163

    Article  CAS  PubMed  Google Scholar 

  29. Fazekas F, Kleinert R, Offenbacher H et al (1991) The morphologic correlate of incidental punctate white matter hyperintensities on MR images. Am J Neuroradiol 12:915–921

    CAS  PubMed  Google Scholar 

  30. Bombardier C, Gladman D, Urowitz M, Caron D, Chang CH (1992) Derivation of the SLEDAI: a disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640

    Article  CAS  PubMed  Google Scholar 

  31. Liu T, Khalidov I, de Rochefort L et al (2011) A novel background field removal method for MRI using projection onto dipole fields (PDF). NMR Biomed 24:1129–1136

    Article  PubMed  PubMed Central  Google Scholar 

  32. Jin L, Wang J, Zhao L et al (2011) Decreased serum ceruloplasmin levels characteristically aggravate nigral iron deposition in Parkinson’s disease. Brain 134:50–58

    Article  PubMed  Google Scholar 

  33. Lim MK, Suh CH, Kim HJ et al (2000) Systemic lupus erythematosus: brain MR imaging and single-voxel hydrogen 1 MR spectroscopy. Radiology 217:43–49

    Article  CAS  PubMed  Google Scholar 

  34. Jung RE, Caprihan A, Chavez RS et al (2010) Diffusion tensor imaging in neuropsychiatric systemic lupus erythematosus. BMC Neurol 10:65

    Article  PubMed  PubMed Central  Google Scholar 

  35. Roldan CA, Shively BK, Crawford MH (1996) An echocardiographic study of valvular heart disease associated with systemic lupus erythematosus. N Engl J Med 335:1424–1430

    Article  CAS  PubMed  Google Scholar 

  36. Moore PM, Lisak RP (1996) Systemic lupus erythematosus: immunopathogenesis of neurologic dysfunction. Springer Semin Immunoneurol 17:43–60

    Google Scholar 

  37. Campbell A, Smith MA, Sayre LM, Bondy SC, Perry G (2001) Mechanisms by which metals promote events connected to neurodegenerative diseases. Brain Res Bull 55:125–132

    Article  CAS  PubMed  Google Scholar 

  38. Hallgren B, Sourander P (1958) The effect of age on the non-haemin iron in the human brain. J Neurochem 3:41–51

    Article  CAS  PubMed  Google Scholar 

  39. Takanashi J-I, Barkovich AJ, Dillon WP, Sherr EH, Hart KA, Packman S (2003) T1 hyperintensity in the pulvinar: key imaging feature for diagnosis of Fabry disease. Am J Neuroradiol 24:916–921

    PubMed  Google Scholar 

  40. Langkammer C, Krebs N, Goessler W et al (2010) Quantitative MR imaging of brain iron: a postmortem validation study. Radiology 257:455–462

    Article  PubMed  Google Scholar 

  41. Pauling L, Coryell CD (1936) The magnetic properties and structure of hemoglobin, oxyhemoglobin and carbonmonoxyhemoglobin. Proc Natl Acad Sci U S A 22:210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The scientific guarantor of this publication is Yukunori Korogi M.D. The authors of this manuscript declare relationships with the following companies: Y. Tanaka has received consulting fees, speaking fees and/or honoraria from Abbvie, Chugai, Astellas, Takeda, Santen, Mitsubishi-Tanabe, Pfizer, Janssen, Eisai, Daiichi-Sankyo, UCB, GlaxoSmithKline, Bristol-Myers and has received research grants from Mitsubishi-Tanabe, Chugai, MSD, Astellas, Novartis. The other authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional review board approval was obtained. Written informed consent was waived by the institutional review board. Methodology: retrospective case-control study performed at one institution.

Author information

Authors and Affiliations

  1. Department of Radiology, University of Occupational and Environmental Health, School of Medicine, 1-1 Iseigaoka, Yahatanishi-ku, Kitakyushu, 807-8555, Japan

    Atsushi Ogasawara, Shingo Kakeda, Keita Watanabe, Satoru Ide, Issei Ueda, Yu Murakami, Junji Moriya, Koichiro Futatsuya, Toru Sato & Yukunori Korogi

  2. The First Department of Internal Medicine, University of Occupational and Environmental Health, School of Medicine, 1-1 Iseigaoka, Yahatanishi-ku, Kitakyushu, 807-8555, Japan

    Shingo Nakayamada, Kazuyoshi Saito & Yoshiya Tanaka

  3. Departments of Biomedical Engineering and Radiology, Cornell University, MedImageMetric LLC, New York, NY, 10044, USA

    Tian Liu & Yi Wang

Authors
  1. Atsushi Ogasawara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shingo Kakeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keita Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Satoru Ide
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Issei Ueda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Junji Moriya
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Koichiro Futatsuya
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Toru Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shingo Nakayamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kazuyoshi Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yoshiya Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Tian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Yukunori Korogi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shingo Kakeda.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ogasawara, A., Kakeda, S., Watanabe, K. et al. Quantitative susceptibility mapping in patients with systemic lupus erythematosus: detection of abnormalities in normal-appearing basal ganglia. Eur Radiol 26, 1056–1063 (2016). https://doi.org/10.1007/s00330-015-3929-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-015-3929-3

Keywords

Search

Navigation