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Challenges and Opportunities in dMRI Data Harmonization

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Computational Diffusion MRI (MICCAI 2019)

Abstract

Advances in diffusion MRI (dMRI) have led to discoveries of factors that affect brain microstructure and connectivity in health and disease. The small size of many neuroimaging studies led to concerns about poor reproducibility of research findings, and calls for the comparison and pooling of multi-cohort datasets to establish the consistency of reported effects. Across studies diffusion MRI protocols vary in spatial, angular and q-space resolution, b-value, as well as hardware used—all of which affect measured diffusion parameters. Efforts to compare and pool dMRI measures use meta- or mega- analytical techniques to compensate for these sources of variance. Meta-analytical methods gauge the consistency of effects, and mega-analytical methods involve mathematical or statistical transformations of the data. Here, we review some recent advances that allowed the diffusion community to create large scale population studies with greater rigor and generalizability than was previously attainable by individual studies.

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Notes

  1. 1.

    https://grants.nih.gov/reproducibility/index.htm.

  2. 2.

    This assumption is not necessarily true for either type of phantom: for the human phantom, slight brain morphometry changes have been observed in the course of a day [45], and repeat scans on the same scanner will not be identical; for a manufactured phantom, transportation of the phantom may affect its geometry.

References

  1. Goodman, S.N., Fanelli, D., Ioannidis, J.P.: What does research reproducibility mean? Sci. Transl. Med. 8(341), 341ps12 (2016)

    Article  Google Scholar 

  2. Munafò, M.R., Nosek, B.A., Bishop, D.V., Button, K.S., et al.: A manifesto for reproducible science. Sci. Transl. Med. 1(1), 0021 (2017)

    Google Scholar 

  3. Gilmore, R.O., Diaz, M.T., Wyble, B.A., Yarkoni, T.: Progress toward openness, transparency, and reproducibility in cognitive neuroscience. Ann. N. Y. Acad. Sci. 1396(1), 5–18 (2017)

    Article  Google Scholar 

  4. Kelly, S., Jahanshad, N., et al.: Widespread white matter microstructural differences in schizophrenia across 4322 individuals: results from the ENIGMA Schizophrenia DTI Working Group. Mol. Psychiatry (2017)

    Google Scholar 

  5. Button, K.S., Ioannidis, J.P., Mokrysz, C., Nosek, B.A., Flint, J., Robinson, E.S., Munafò, M.R.: Power failure: why small sample size undermines the reliability of neuroscience. Nat. Rev. Neurosci. 14(5), 365 (2013)

    Article  Google Scholar 

  6. Ioannidis, J.P., Greenland, S., Hlatky, M.A., Khoury, M.J., Macleod, M.R., Moher, D., Schulz, K.F., Tibshirani, R.: Increasing value and reducing waste in research design, conduct, and analysis. Lancet 383(9912), 166–175 (2014)

    Article  Google Scholar 

  7. Eklund, A., Nichols, T.E., Knutsson, H.: Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc. Natl. Acad. Sci. 201602413 (2016)

    Google Scholar 

  8. Smith, S.M., Nichols, T.E.: Statistical challenges in “Big Data” human neuroimaging. Neuron 97(2), 263–268 (2018)

    Article  Google Scholar 

  9. Miller, K.L., Alfaro-Almagro, F., Bangerter, N.K., Thomas, D.L., et al.: Multimodal population brain imaging in the UK Biobank prospective epidemiological study. Nat. Neurosci. 19(11), 1523 (2016)

    Article  Google Scholar 

  10. Hibar, D.P., Stein, J.L., Renteria, M.E., et al.: Common genetic variants influence human subcortical brain structures. Nature 520(7546), 224 (2015)

    Article  Google Scholar 

  11. Jack Jr., C.R., Barnes, J., Bernstein, M.A., Borowski, B.J., Brewer, J., et al.: Magnetic resonance imaging in Alzheimer’s disease neuroimaging initiative 2. Alzheimer’s Dement. 11(7), 740–756 (2015)

    Article  Google Scholar 

  12. Weiner, M.W., Veitch, D.P., Aisen, P.S., Beckett, L.A., Cairns, N.J., et al.: Impact of the Alzheimer’s disease neuroimaging initiative, 2004 to 2014. Alzheimer’s Dement. 11(7), 865–884 (2015)

    Article  Google Scholar 

  13. Marek, K., Jennings, D., Lasch, S., Siderowf, A., et al.: The parkinson progression marker initiative (PPMI). Prog. Neurobiol. 95(4), 629–635 (2011)

    Article  Google Scholar 

  14. Vollmar, C., O’Muircheartaigh, J., Barker, G.J., Identical, et al.: but not the same: intra-site and inter-site reproducibility of fractional anisotropy measures on two 3.0 t scanners. NeuroImage 51(4), 1384–1394 (2010)

    Article  Google Scholar 

  15. Pohl, K.M., Sullivan, E.V., Rohlfing, T., et al.: Harmonizing DTI measurements across scanners to examine the development of white matter microstructure in 803 adolescents of the NCANDA study. NeuroImage 130, 194–213 (2016)

    Article  Google Scholar 

  16. El-Sharkawy, A.M., Schär, M., Bottomley, P.A., Atalar, E.: Monitoring and correcting spatio-temporal variations of the MR scanner’s static magnetic field. Magn. Reson. Mater. Phys. Biol. Med. 19(5), 223–236 (2006)

    Article  Google Scholar 

  17. Vos, S.B., Tax, C.M., Luijten, P.R., et al.: The importance of correcting for signal drift in diffusion MRI. Magn. Reson. Med. 77(1), 285–299 (2017)

    Article  Google Scholar 

  18. Foerster, B.U., Tomasi, D., Caparelli, E.C.: Magnetic field shift due to mechanical vibration in functional magnetic resonance imaging. Magn. Reson. Med. Off. J. ISMRM 54(5), 1261–1267 (2005)

    Article  Google Scholar 

  19. Benner, T., van der Kouwe, A.J., et al.: Real-time RF pulse adjustment for B0 drift correction. Magn. Reson. Med. Off. J. ISMRM 56(1), 204–209 (2006)

    Article  Google Scholar 

  20. White, T., Magnotta, V.A., Bockholt, H.J., et al.: Global white matter abnormalities in schizophrenia: a multisite diffusion tensor imaging study. Schizophr. Bull. 37(1), 222–232 (2009)

    Article  Google Scholar 

  21. Brander, A., Kataja, A., Saastamoinen, A., et al.: Diffusion tensor imaging of the brain in a healthy adult population: Normative values and measurement reproducibility at 3 T and 1.5 T. Acta Radiol. 51(7), 800–807 (2010)

    Article  Google Scholar 

  22. Pagani, E., Hirsch, J.G., Pouwels, P.J., et al.: Intercenter differences in diffusion tensor MRI acquisition. J. Magn. Reson. Imaging 31(6), 1458–1468 (2010)

    Article  Google Scholar 

  23. Zhan, L., Mueller, B.A., Jahanshad, N., et al.: Magnetic resonance field strength effects on diffusion measures and brain connectivity networks. Brain Connect. 3(1), 72–86 (2013)

    Article  Google Scholar 

  24. Papinutto, N.D., Maule, F., Jovicich, J.: Reproducibility and biases in high field brain diffusion MRI: an evaluation of acquisition and analysis variables. Magn. Reson. Imaging 31(6), 827–839 (2013)

    Article  Google Scholar 

  25. Bisdas, S., et al.: Reproducibility, interrater agreement, and age-related changes of fractional anisotropy measures at 3t in healthy subjects: effect of the applied b-value. Am. J. Neuroradiol. 29(6), 1128–1133 (2008)

    Article  Google Scholar 

  26. Correia, M.M., Carpenter, T.A., Williams, G.B.: Looking for the optimal DTI acquisition scheme given a maximum scan time: are more b-values a waste of time? Magn. Reson. Imaging 27(2), 163–175 (2009)

    Article  Google Scholar 

  27. Giannelli, M., Cosottini, M., et al.: Dependence of brain DTI maps of fractional anisotropy and mean diffusivity on the number of diffusion weighting directions. J. Appl. Clin. Med. Phys. 11(1), 176–190 (2010)

    Article  Google Scholar 

  28. Zhan, L., Leow, A.D., Jahanshad, N., et al.: How does angular resolution affect diffusion imaging measures? NeuroImage 49(2), 1357–1371 (2010)

    Article  Google Scholar 

  29. Zhan, L., Franc, D., Patel, V., et al.: How do spatial and angular resolution affect brain connectivity maps from diffusion MRI? In: 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI), pp. 1–4. IEEE (2012)

    Google Scholar 

  30. Jahanshad, N., et al.: Diffusion tensor imaging in seven minutes: determining trade-offs between spatial and directional resolution. In: 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro, pp. 1161–1164. IEEE (2010)

    Google Scholar 

  31. Zhu, T., Hu, R., Qiu, X., et al.: Quantification of accuracy and precision of multi-center DTI measurements: a diffusion phantom and human brain study. NeuroImage 56(3), 1398–1411 (2011)

    Article  Google Scholar 

  32. McGibney, G., Smith, M., Nichols, S., Crawley, A.: Quantitative evaluation of several partial fourier reconstruction algorithms used in MRI. Magn. Reson. Med. 30(1), 51–59 (1993)

    Article  Google Scholar 

  33. Jovicich, J., Marizzoni, M., Bosch, B., et al.: Multisite longitudinal reliability of tract-based spatial statistics in diffusion tensor imaging of healthy elderly subjects. NeuroImage 101, 390–403 (2014)

    Article  Google Scholar 

  34. Teipel, S.J., Reuter, S., Stieltjes, B., et al.: Multicenter stability of diffusion tensor imaging measures: a European clinical and physical phantom study. Psychiatry Res. Neuroimaging 194(3), 363–371 (2011)

    Article  Google Scholar 

  35. Wolz, R., Schwarz, A.J., Yu, P., et al.: Robustness of automated hippocampal volumetry across magnetic resonance field strengths and repeat images. Alzheimer’s Dement. 10(4), 430–438 (2014)

    Article  Google Scholar 

  36. Thompson, P.M., Stein, J.L., Medland, S.E., et al.: The ENIGMA consortium: large-scale collaborative analyses of neuroimaging and genetic data. Brain Imaging Behav. 8(2), 153–182 (2014)

    Google Scholar 

  37. Thompson, P.M., Andreassen, O.A., Arias-Vasquez, A., et al.: ENIGMA and the individual: predicting factors that affect the brain in 35 countries worldwide. NeuroImage 145, 389–408 (2017)

    Article  Google Scholar 

  38. Jahanshad, N., Kochunov, P.V., Sprooten, E., et al.: Multi-site genetic analysis of diffusion images and voxelwise heritability analysis: a pilot project of the ENIGMA-DTI working group. NeuroImage 81, 455–469 (2013)

    Article  Google Scholar 

  39. Boedhoe, P.S., Schmaal, L., Abe, Y., et al.: Distinct subcortical volume alterations in pediatric and adult OCD: a worldwide meta-and mega-analysis. Am. J. Psychiatry 174(1), 60–69 (2016)

    Google Scholar 

  40. Jahanshad, N., Ganjgahi, H., Bralten, J., et al.: Do candidate genes affect the brain’s white matter microstructure? Large-scale evaluation of 6,165 diffusion MRI scans. BioRxiv 107987 (2017)

    Google Scholar 

  41. Oehlert, G.W.: A first course in design and analysis of experiments (2010)

    Google Scholar 

  42. Bates, D., Mächler, M., Bolker, B., Walker, S.: Fitting linear mixed-effects models using lme4 (2014). arXiv preprint arXiv:1406.5823

  43. Nir, T.M., Jahanshad, N., Villalon-Reina, J.E., et al.: Fractional anisotropy derived from the diffusion tensor distribution function boosts power to detect alzheimer’s disease deficits. Magn. Reson. Med. 78(6), 2322–2333 (2017)

    Article  Google Scholar 

  44. Nir, T.M., Jahanshad, N., Villalon-Reina, J.E., et al.: Effectiveness of regional DTI measures in distinguishing Alzheimer’s disease, MCI, and normal aging. NeuroImage Clin. 3, 180–195 (2013)

    Article  Google Scholar 

  45. Trefler, A., Sadeghi, N., Thomas, A.G., Pierpaoli, C., Baker, C.I., Thomas, C.: Impact of time-of-day on brain morphometric measures derived from T1-weighted magnetic resonance imaging. NeuroImage 133, 41–52 (2016)

    Article  Google Scholar 

  46. Clarkson, M.J., Ourselin, S., et al.: Comparison of phantom and registration scaling corrections using the ADNI cohort. NeuroImage 47(4), 1506–1513 (2009)

    Article  Google Scholar 

  47. Venkatraman, V.K., Gonzalez, C.E., Landman, B., et al.: Region of interest correction factors improve reliability of diffusion imaging measures within and across scanners and field strengths. NeuroImage 119, 406–416 (2015)

    Article  Google Scholar 

  48. Kochunov, P., Jahanshad, N., Sprooten, E., et al.: Multi-site study of additive genetic effects on fractional anisotropy of cerebral white matter: comparing meta and megaanalytical approaches for data pooling. NeuroImage 95, 136–150 (2014)

    Article  Google Scholar 

  49. Fortin, J.P., Parker, D., Tunc, B., et al.: Harmonization of multi-site diffusion tensor imaging data. NeuroImage 161, 149–170 (2017)

    Article  Google Scholar 

  50. Johnson, W.E., Li, C., Rabinovic, A.: Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8(1), 118–127 (2007)

    Article  MATH  Google Scholar 

  51. Li, C., Wong, W.H.: DNA-chip analyzer (dChip). In: The Analysis of Gene Expression, pp. 120–141. Springer, New York (2003)

    Google Scholar 

  52. Parvathaneni, P., Bao, S., Hainline, A., Huo, Y., et al.: Harmonization of white and gray matter features in diffusion microarchitecture for cross sectional studies. Medical Image Analysis. Springer (2018)

    Google Scholar 

  53. Yeatman, J.D., Wandell, B.A., Mezer, A.A.: Lifespan maturation and degeneration of human brain white matter. Nat. Commun. 5, 4932 (2014)

    Article  Google Scholar 

  54. Bava, S., Boucquey, V., Goldenberg, D., et al.: Sex differences in adolescent white matter architecture. Brain Res. 1375, 41–48 (2011)

    Article  Google Scholar 

  55. Hasan, K.M., Kamali, A., Abid, H., Kramer, L.A., Fletcher, J.M., Ewing-Cobbs, L.: Quantification of the spatiotemporal microstructural organization of the human brain association, projection and commissural pathways across the lifespan using diffusion tensor tractography. Brain Struct. Funct. 214(4), 361–373 (2010)

    Article  Google Scholar 

  56. Herting, M.M., et al.: The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cereb. Cortex 22(9), 1979–1992 (2011)

    Article  Google Scholar 

  57. Wang, Y., Adamson, C., Yuan, W., et al.: Sex differences in white matter development during adolescence: a DTI study. Brain Res. 1478, 1–15 (2012)

    Article  Google Scholar 

  58. Kochunov, P., Dickie, E.W., Viviano, J.D., et al.: Integration of routine QA data into mega-analysis may improve quality and sensitivity of multisite diffusion tensor imaging studies. Hum. Brain Mapp. 39(2), 1015–1023 (2018)

    Article  Google Scholar 

  59. Mirzaalian, H., Ning, L., et al.: Multi-site harmonization of diffusion MRI data in a registration framework. Brain Imaging Behav. 12(1), 284–295 (2018)

    Article  Google Scholar 

  60. Drobnjak, I., Gavaghan, D., et al.: Development of a functional magnetic resonance imaging simulator for modeling realistic rigid-body motion artifacts. Magn. Reson. Med. Off. J. ISMRM 56(2), 364–380 (2006)

    Article  Google Scholar 

  61. Graham, M.S., et al.: Realistic simulation of artefacts in diffusion MRI for validating post-processing correction techniques. NeuroImage 125, 1079–1094 (2016)

    Article  Google Scholar 

  62. Maier-Hein, K.H., Neher, P.F., et al.: The challenge of mapping the human connectome based on diffusion tractography. Nat. Commun. 8(1), 1349 (2017)

    Article  Google Scholar 

  63. Tax, C.M., Grussu, F., Kaden, E., et al.: Cross-vendor and cross-protocol harmonisation of diffusion MRI data: a comparative study. In: ISMRM (2017)

    Google Scholar 

  64. Zhan, L., Zhou, J., Wang, Y., et al.: Comparison of nine tractography algorithms for detecting abnormal structural brain networks in Alzheimer’s disease. Front. Aging Neurosci. 7, 48 (2015)

    Article  Google Scholar 

  65. Zhan, L., Liu, Y., Wang, Y., et al.: Boosting brain connectome classification accuracy in Alzheimer’s disease using higher-order singular value decomposition. Front. Neurosci. 9, 257 (2015)

    Google Scholar 

  66. Villalon-Reina, J., Nir, T., et al.: Reliability of structural connectivity examined with four different diffusion reconstruction methods at two different spatial and angular resolutions. In: Computational Diffusion MRI, pp. 219–231. Springer, Cham (2016)

    Chapter  Google Scholar 

  67. Bengio, Y., et al.: Learning deep architectures for AI. Found. Trends®. Mach. Learn. 2(1), 1–127 (2009)

    Article  MathSciNet  MATH  Google Scholar 

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Acknowledgements

The work was supported in part by U54 EB020403. Additional support was provided by R01MH116147, P41 EB015922, RF1 AG051710, RF1 AG041915 and and Michael J. Fox Foundation grant 14848.

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Correspondence to Neda Jahanshad .

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Zhu, A.H., Moyer, D.C., Nir, T.M., Thompson, P.M., Jahanshad, N. (2019). Challenges and Opportunities in dMRI Data Harmonization. In: Bonet-Carne, E., Grussu, F., Ning, L., Sepehrband, F., Tax, C. (eds) Computational Diffusion MRI. MICCAI 2019. Mathematics and Visualization. Springer, Cham. https://doi.org/10.1007/978-3-030-05831-9_13

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