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MRI quality control for the Italian Neuroimaging Network Initiative: moving towards big data in multiple sclerosis

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Abstract

The Italian Neuroimaging Network Initiative (INNI) supports the creation of a repository, where MRI, clinical, and neuropsychological data from multiple sclerosis (MS) patients and healthy controls are collected from Italian Research Centers with internationally recognized expertise in MRI applied to MS. However, multicenter MRI data integration needs standardization and quality control (QC). This study aimed to implement quantitative measures for characterizing the standardization and quality of MRI collected within INNI. MRI scans of 423 MS patients, including 3D T1- and T2-weighted, were obtained from INNI repository (from Centers A, B, C, and D). QC measures were implemented to characterize: (1) head positioning relative to the magnet isocenter; (2) intensity inhomogeneity; (3) relative image contrast between brain tissues; and (4) image artefacts. Centers A and D showed the most accurate subject positioning within the MR scanner (median z-offsets = − 2.6 ± 1.7 cm and − 1.1 ± 2 cm). A low, but significantly different, intensity inhomogeneity on 3D T1-weighted MRI was found between all centers (p < 0.05), except for Centers A and C that showed comparable image bias fields. Center D showed the highest relative contrast between gray and normal appearing white matter (NAWM) on 3D T1-weighed MRI (0.63 ± 0.04), while Center B showed the highest relative contrast between NAWM and MS lesions on FLAIR (0.21 ± 0.06). Image artefacts were mainly due to brain movement (60%) and ghosting (35%). The implemented QC procedure ensured systematic data quality assessment within INNI, thus making available a huge amount of high-quality MRI to better investigate pathophysiological substrates and validate novel MRI biomarkers in MS.

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References

  1. Advanced Normalization Toolbox website: http://stnava.github.io/ANTs/

  2. Alfaro-Almagro F, Jenkinson M, Bangerter NK, Andersson JLR, Griffanti L, Douaud G, Sotiropoulos SN, Jbabdi S, Hernandez-Fernandez M, Vallee E, Vidaurre D, Webster M, McCarthy P, Rorden C, Daducci A, Alexander DC, Zhang H, Dragonu I, Matthews PM, Miller KL, Smith SM (2018) Image processing and quality control for the first 10,000 brain imaging datasets from UK biobank. Neuroimage 166:400–424

    PubMed  Google Scholar 

  3. Baldwin LN, Wachowicz K, Thomas SD, Rivest R, Fallone BG (2007) Characterization, prediction, and correction of geometric distortion in 3 T MR images. Med Phys 34:388–399

    PubMed  Google Scholar 

  4. Bennett CM, Miller MB (2010) How reliable are the results from functional magnetic resonance imaging? Ann N Y Acad Sci 1191:133–155

    PubMed  Google Scholar 

  5. Bernstein MAHJ, Ward HA (2006) Imaging artifacts at 3.0T. J Magn Reson Imaging 24:735–746

    PubMed  Google Scholar 

  6. Blumenthal JD, Zijdenbos A, Molloy E, Giedd JN (2002) Motion artifact in magnetic resonance imaging: implications for automated analysis. Neuroimage 16:89–92

    PubMed  Google Scholar 

  7. Brown JA, Van Horn JD (2016) Connected brains and minds—the UMCD repository for brain connectivity matrices. Neuroimage 124:1238–1241

    PubMed  Google Scholar 

  8. Choudhri AF, Chin EM, Klimo P, Boop FA (2014) Spatial distortion due to field inhomogeneity in 3.0 tesla intraoperative MRI. Neuroradiol J 27:387–392

    PubMed  PubMed Central  Google Scholar 

  9. Despotovic I, Goossens B, Philips W (2015) MRI segmentation of the human brain: challenges, methods, and applications. Comput Math Methods Med 2015:450341

    PubMed  PubMed Central  Google Scholar 

  10. Dietrich O, Raya JG, Reeder SB, Reiser MF, Schoenberg SO (2007) Measurement of signal-to-noise ratios in MR images: influence of multichannel coils, parallel imaging, and reconstruction filters. J Magn Reson Imaging 26:375–385

    PubMed  Google Scholar 

  11. Eickhoff S, Nichols TE, Van Horn JD, Turner JA (2016) Sharing the wealth: neuroimaging data repositories. Neuroimage 124:1065–1068

    PubMed  Google Scholar 

  12. Filippi M, Bar-Or A, Piehl F, Preziosa P, Solari A, Vukusic S, Rocca MA (2018) Multiple sclerosis. Nat Rev Dis Primers 4:43

    PubMed  Google Scholar 

  13. Filippi M, Preziosa P, Rocca MA (2017) Microstructural MR imaging techniques in multiple sclerosis. Neuroimaging Clin N Am 27:313–333

    PubMed  Google Scholar 

  14. Filippi M, Rocca MA, Bastianello S, Comi G, Gallo P, Gallucci M, Ghezzi A, Marrosu MG, Minonzio G, Pantano P, Pozzilli C, Tedeschi G, Trojano M, Falini A, De Stefano N, Neuroimaging, Neurology MSSGotISo, Functional Neuroradiology Section of the Italian Association of N (2013) Guidelines from the Italian neurological and neuroradiological societies for the use of magnetic resonance imaging in daily life clinical practice of multiple sclerosis patients. Neurol Sci 34:2085–2093

    PubMed  Google Scholar 

  15. Filippi M, Rocca MA, Ciccarelli O, De Stefano N, Evangelou N, Kappos L, Rovira A, Sastre-Garriga J, Tintore M, Frederiksen JL, Gasperini C, Palace J, Reich DS, Banwell B, Montalban X, Barkhof F, Group MS (2016) MRI criteria for the diagnosis of multiple sclerosis: MAGNIMS consensus guidelines. Lancet Neurol 15:292–303

    PubMed  PubMed Central  Google Scholar 

  16. Filippi M, Tedeschi G, Pantano P, De Stefano N, Zaratin P, Rocca MA, Network I (2017) The Italian neuroimaging network initiative (INNI): enabling the use of advanced MRI techniques in patients with MS. Neurol Sci 38:1029–1038

    CAS  PubMed  Google Scholar 

  17. Gedamu E (2011) Guidelines for developing automated quality control procedures for brain magnetic resonance images acquired in multi-centre clinical trials. Appl Exp Qual Control 26:135–158

    Google Scholar 

  18. Glover GH, Mueller BA, Turner JA, van Erp TG, Liu TT, Greve DN, Voyvodic JT, Rasmussen J, Brown GG, Keator DB, Calhoun VD, Lee HJ, Ford JM, Mathalon DH, Diaz M, O’Leary DS, Gadde S, Preda A, Lim KO, Wible CG, Stern HS, Belger A, McCarthy G, Ozyurt B, Potkin SG (2012) Function biomedical informatics research network recommendations for prospective multicenter functional MRI studies. J Magn Reson Imaging 36:39–54

    PubMed  PubMed Central  Google Scholar 

  19. Gorgolewski KJ, Varoquaux G, Rivera G, Schwartz Y, Sochat VV, Ghosh SS, Maumet C, Nichols TE, Poline JB, Yarkoni T, Margulies DS, Poldrack RA (2016) NeuroVault.org: a repository for sharing unthresholded statistical maps, parcellations, and atlases of the human brain. Neuroimage 124:1242–1244

    PubMed  Google Scholar 

  20. Janke A, Zhao H, Cowin GJ, Galloway GJ, Doddrell DM (2004) Use of spherical harmonic deconvolution methods to compensate for nonlinear gradient effects on MRI images. Magn Reson Med 52:115–122

    PubMed  Google Scholar 

  21. Jovicich J, Czanner S, Greve D, Haley E, van der Kouwe A, Gollub R, Kennedy D, Schmitt F, Brown G, Macfall J, Fischl B, Dale A (2006) Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage 30:436–443

    PubMed  Google Scholar 

  22. Landhuis E (2017) Neuroscience: big brain, big data. Nature 541:559–561

    CAS  PubMed  Google Scholar 

  23. Marcus DS, Harms MP, Snyder AZ, Jenkinson M, Wilson JA, Glasser MF, Barch DM, Archie KA, Burgess GC, Ramaratnam M, Hodge M, Horton W, Herrick R, Olsen T, McKay M, House M, Hileman M, Reid E, Harwell J, Coalson T, Schindler J, Elam JS, Curtiss SW, Van Essen DC, Consortium WU-MH (2013) Human Connectome Project informatics: quality control, database services, and data visualization. Neuroimage 80:202–219

    PubMed  Google Scholar 

  24. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, McFarland HF, Paty DW, Polman CH, Reingold SC, Sandberg-Wollheim M, Sibley W, Thompson A, van den Noort S, Weinshenker BY, Wolinsky JS (2001) Recommended diagnostic criteria for multiple sclerosis: guidelines from the international panel on the diagnosis of multiple sclerosis. Ann Neurol 50:121–127

    CAS  PubMed  Google Scholar 

  25. Miller KL, Alfaro-Almagro F, Bangerter NK, Thomas DL, Yacoub E, Xu J, Bartsch AJ, Jbabdi S, Sotiropoulos SN, Andersson JL, Griffanti L, Douaud G, Okell TW, Weale P, Dragonu I, Garratt S, Hudson S, Collins R, Jenkinson M, Matthews PM, Smith SM (2016) Multimodal population brain imaging in the UK Biobank prospective epidemiological study. Nat Neurosci 19:1523–1536

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Petersen RC, Aisen PS, Beckett LA, Donohue MC, Gamst AC, Harvey DJ, Jack CR Jr, Jagust WJ, Shaw LM, Toga AW, Trojanowski JQ, Weiner MW (2010) Alzheimer’s disease neuroimaging initiative (ADNI): clinical characterization. Neurology 74:201–209

    PubMed  PubMed Central  Google Scholar 

  27. Pham DL, Xu C, Prince JL (2000) Current methods in medical image segmentation. Annu Rev Biomed Eng 2:315–337

    CAS  PubMed  Google Scholar 

  28. Poldrack RA, Gorgolewski KJ (2014) Making big data open: data sharing in neuroimaging. Nat Neurosci 17:1510–1517

    CAS  PubMed  Google Scholar 

  29. Reid AT, Bzdok D, Genon S, Langner R, Muller VI, Eickhoff CR, Hoffstaedter F, Cieslik EC, Fox PT, Laird AR, Amunts K, Caspers S, Eickhoff SB (2016) ANIMA: a data-sharing initiative for neuroimaging meta-analyses. Neuroimage 124:1245–1253

    PubMed  Google Scholar 

  30. Reuter M, Tisdall MD, Qureshi A, Buckner RL, van der Kouwe AJW, Fischl B (2015) Head motion during MRI acquisition reduces gray matter volume and thickness estimates. Neuroimage 107:107–115

    PubMed  Google Scholar 

  31. Rocca MA, Battaglini M, Benedict RH, De Stefano N, Geurts JJ, Henry RG, Horsfield MA, Jenkinson M, Pagani E, Filippi M (2017) Brain MRI atrophy quantification in MS: from methods to clinical application. Neurology 88:403–413

    PubMed  PubMed Central  Google Scholar 

  32. Rocca MA, Filippi M (2007) Functional MRI in multiple sclerosis. J Neuroimaging 17(Suppl 1):36S–41S

    PubMed  Google Scholar 

  33. Rovira À (2012) Segmentation of multiple sclerosis lesions in brain MRI: a review of automated approaches. Inf Sci 186:164–185

    Google Scholar 

  34. Roy S, Carass A, Prince J (2011) A compressed sensing approach for MR tissue contrast synthesis. Inf Process Med Imaging 22:371–383

    PubMed  PubMed Central  Google Scholar 

  35. Elhdnmkha S (2004) A short overview of MRI artefacts. SA J Radiol 8:13–17

    Google Scholar 

  36. Saranathan M, Tourdias T, Kerr AB, Bernstein JD, Kerchner GA, Han MH, Rutt BK (2014) Optimization of magnetization-prepared 3-dimensional fluid attenuated inversion recovery imaging for lesion detection at 7 T. Invest Radiol 49:290–298

    PubMed  PubMed Central  Google Scholar 

  37. Seibert TM, White NS, Kim GY, Moiseenko V, McDonald CR, Farid N, Bartsch H, Kuperman J, Karunamuni R, Marshall D, Holland D, Sanghvi P, Simpson DR, Mundt AJ, Dale AM, Hattangadi-Gluth JA (2016) Distortion inherent to magnetic resonance imaging can lead to geometric miss in radiosurgery planning. Pract Radiat Oncol 6:e319–e328

    PubMed  PubMed Central  Google Scholar 

  38. Sudlow C, Gallacher J, Allen N, Beral V, Burton P, Danesh J, Downey P, Elliott P, Green J, Landray M, Liu B, Matthews P, Ong G, Pell J, Silman A, Young A, Sprosen T, Peakman T, Collins R (2015) UK biobank: an open access resource for identifying the causes of a wide range of complex diseases of middle and old age. PLoS Med 12:e1001779

    PubMed  PubMed Central  Google Scholar 

  39. Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, Correale J, Fazekas F, Filippi M, Freedman MS, Fujihara K, Galetta SL, Hartung HP, Kappos L, Lublin FD, Marrie RA, Miller AE, Miller DH, Montalban X, Mowry EM, Sorensen PS, Tintore M, Traboulsee AL, Trojano M, Uitdehaag BMJ, Vukusic S, Waubant E, Weinshenker BG, Reingold SC, Cohen JA (2018) Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol 17:162–173

    PubMed  Google Scholar 

  40. Tisdall MD, Reuter M, Qureshi A, Buckner RL, Fischl B, van der Kouwe AJW (2016) Prospective motion correction with volumetric navigators (vNavs) reduces the bias and variance in brain morphometry induced by subject motion. Neuroimage 127:11–22

    PubMed  Google Scholar 

  41. Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, Gee JC (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29:1310–1320

    PubMed  PubMed Central  Google Scholar 

  42. Van Essen DC, Smith SM, Barch DM, Behrens TE, Yacoub E, Ugurbil K, Consortium WU-MH (2013) The WU-Minn human connectome project: an overview. Neuroimage 80:62–79

    PubMed  Google Scholar 

  43. Van Horn JD, Toga AW (2014) Human neuroimaging as a “Big Data” science. Brain Imaging Behav 8:323–331

    PubMed  PubMed Central  Google Scholar 

  44. Vargas MI, Delavelle J, Kohler R, Becker CD, Lovblad K (2009) Brain and spine MRI artifacts at 3Tesla. J Neuroradiol 36:74–81

    CAS  PubMed  Google Scholar 

  45. Vovk U, Pernus F, Likar B (2007) A review of methods for correction of intensity inhomogeneity in MRI. IEEE Trans Med Imaging 26:405–421

    PubMed  Google Scholar 

  46. Wang D, Doddrell DM, Cowin G (2004) A novel phantom and method for comprehensive 3-dimensional measurement and correction of geometric distortion in magnetic resonance imaging. Magn Reson Imaging 22:529–542

    PubMed  Google Scholar 

  47. Weavers PT, Tao S, Trzasko JD, Shu Y, Tryggestad EJ, Gunter JL, McGee KP, Litwiller DV, Hwang KP, Bernstein MA (2017) Image-based gradient non-linearity characterization to determine higher-order spherical harmonic coefficients for improved spatial position accuracy in magnetic resonance imaging. Magn Reson Imaging 38:54–62

    PubMed  Google Scholar 

  48. Webb-Vargas Y, Chen S, Fisher A, Mejia A, Xu Y, Crainiceanu C, Caffo B, Lindquist MA (2017) Big Data and Neuroimaging. Stat Biosci 9:543–558

    PubMed  PubMed Central  Google Scholar 

  49. Weiner MW, Veitch DP, Aisen PS, Beckett LA, Cairns NJ, Green RC, Harvey D, Jack CR, Jagust W, Liu E, Morris JC, Petersen RC, Saykin AJ, Schmidt ME, Shaw L, Shen L, Siuciak JA, Soares H, Toga AW, Trojanowski JQ, Alzheimer’s Disease Neuroimaging I (2013) The Alzheimer’s disease neuroimaging initiative: a review of papers published since its inception. Alzheimers Dement 9:e111–194

    PubMed  PubMed Central  Google Scholar 

  50. Ziemssen T, Rauer S, Stadelmann C, Henze T, Koehler J, Penner IK, Lang M, Poehlau D, Baier-Ebert M, Schieb H, Meuth S (2015) Evaluation of study and patient characteristics of clinical studies in primary progressive multiple sclerosis: a systematic review. PLoS One 10:e0138243

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Zivadinov R, Bergsland N, Korn JR, Dwyer MG, Khan N, Medin J, Price JC, Weinstock-Guttman B, Silva D, Group M-MS (2018) Feasibility of brain atrophy measurement in clinical routine without prior standardization of the MRI protocol: results from MS-MRIUS, a longitudinal observational, multicenter real-world outcome study in patients with relapsing–remitting MS. AJNR Am J Neuroradiol 39:289–295

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This project has been supported by a research grant from the Fondazione Italiana Sclerosi Multipla (FISM2018/S/3), and financed or co-financed with the ‘5 per mille’ public funding.

INNI network: Milan: Paola Valsasina, Mauro Sibilia, Paolo Preziosa; Naples: Antonio Gallo, Alvino Bisecco, Renato Docimo; Rome: Nikolaos Petsas, Serena Ruggieri, Silvia Tommasin; Siena: Maria Laura Stromillo, Riccardo Tappa Brocci.

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Loredana Storelli, Maria A. Rocca, Elisabetta Pagani, and Massimo Filippi. The first draft of the manuscript was written by Loredana Storelli, Maria A. Rocca, Elisabetta Pagani, and Massimo Filippi, and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Massimo Filippi.

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Conflicts of interest

L Storelli, P. Pantano, E. Pagani, G. Tedeschi, and P. Zaratin have nothing to disclose. M.A. Rocca received speaker’s honoraria from Biogen Idec, Novartis, Genzyme, Sanofi-Aventis, Teva, Merck Serono, and Roche and receives research support from the Italian Ministry of Health and Fondazione Italiana Sclerosi Multipla. N. De Stefano has received honoraria from Schering, Biogen Idec, Teva, Novartis, Genzyme, and Merck Serono S.A. for consulting services, and speaking and travel support. He serves on advisory boards for Biogen-Idec Merck Serono S.A. and Novartis. M. Filippi is Editor-in-Chief of the Journal of Neurology; received compensation for consulting services and/or speaking activities from Biogen Idec, Merck Serono, Novartis, Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Merck Serono, Novartis, Teva Pharmaceutical Industries, Roche, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, and ARiSLA (Fondazione Italiana di Ricerca per la SLA).

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Ethical approval was received from the local ethical standards committee of each participating Center, and written informed consent was obtained from all participants at the time of data acquisition.

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Storelli, L., Rocca, M.A., Pantano, P. et al. MRI quality control for the Italian Neuroimaging Network Initiative: moving towards big data in multiple sclerosis. J Neurol 266, 2848–2858 (2019). https://doi.org/10.1007/s00415-019-09509-4

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