ENIGMA-DTI; diffusion tensor imaging; fractional anisotropy; reproducibility; white matter microstructure
Abstract :
[en] BACKGROUND: In preparation for longitudinal analyses of white matter development in youths with family histories of substance use disorders (FH+) or without such histories (FH-), we examined the reproducibility and reliability of global and regional measures of fractional anisotropy (FA) values, measured using the Enhancing Neuro Imaging Genetics Through Meta Analysis (ENIGMA)-diffusion tensor imaging (DTI) protocol. Highly reliable measures are necessary to detect any subtle differences in brain development. METHODS: First, we analyzed reproducibility data in a sample of 12 healthy young adults (ages 20-28) imaged three times within a week. Next, we calculated the same metrics in data collected 1-year apart in the sample of 68 FH+ and 21 FH- adolescents. This is a timeframe where within subject changes in white matter microstructure are small compared to between subject variance. Reproducibility was estimated by examining mean coefficients of variation (MCV), mean absolute differences (MAD), and intraclass correlations (ICC) for global and tract-specific FA values. RESULTS: We found excellent reproducibility for whole-brain DTI-FA values and most of the white matter tracts, except for the corticospinal tract and the fornix in both adults and youths. There was no significant effect of FH-group on reproducibility (p = .4). Reproducibility metrics were not significantly different between adolescents and adults (all p > .2). In post hoc analyses, the reproducibility metrics for regional FA values showed a strong positive correlation (r = .6) with the regional FA heritability measures previously reported by ENIGMA-DTI. CONCLUSION: Overall, this study demonstrated an excellent reproducibility of ENIGMA-DTI FA, positing it as viable analysis tools for longitudinal studies and other protocols that repeatedly assess white matter microstructure.
Acheson, A., Wijtenburg, S. A., Rowland, L. M., Bray, B. C., Gaston, F., Mathias, C. W., … Dougherty, D. M. (2014a). Combining diffusion tensor imaging and magnetic resonance spectroscopy to study reduced frontal white matter integrity in youths with family histories of substance use disorders. Human Brain Mapping, 35, 5877–5887.
Acheson, A., Wijtenburg, S. A., Rowland, L. M., Winkler, A. M., Gaston, F., Mathias, C. W., … Kochunov, P. (2014b). Assessment of whole brain white matter integrity in youths and young adults with a family history of substance-use disorders. Human Brain Mapping, 35, 5401–5413.
Bach, M., Laun, F. B., Leemans, A., Tax, C. M., Biessels, G. J., Stieltjes, B., & Maier-Hein, K. H. (2014). Methodological considerations on tract-based spatial statistics (TBSS). NeuroImage, 100, 358–369.
Bartzokis, G., Lu, P. H., Tingus, K., Mendez, M. F., Richard, A., Peters, D. G., … Mintz, J. (2010). Lifespan trajectory of myelin integrity and maximum motor speed. Neurobiology of Aging, 31, 1554–1562.
Barysheva, M., Jahanshad, N., Foland-Ross, L., Altshuler, L. L., & Thompson, P. M. (2013). White matter microstructural abnormalities in bipolar disorder: A whole brain diffusion tensor imaging study. NeuroImage Clinical, 2, 558–568.
Basser, P. J., Mattiello, J., & LeBihan, D. (1994). MR diffusion tensor spectroscopy and imaging. Biophysical Journal, 66, 259–267.
Basser, P. J., & Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. Journal of Magnetic Resonance, 111, 209–219.
Bisdas, S., Bohning, D. E., Besenski, N., Nicholas, J. S., & Rumboldt, Z. (2008). Reproducibility, interrater agreement, and age-related changes of fractional anisotropy measures at 3T in healthy subjects: Effect of the applied b-value. AJNR. American Journal of Neuroradiology, 29, 1128–1133.
Carballedo, A., Amico, F., Ugwu, I., Fagan, A. J., Fahey, C., Morris, D., … Frodl, T. (2012). Reduced fractional anisotropy in the uncinate fasciculus in patients with major depression carrying the met-allele of the Val66Met brain-derived neurotrophic factor genotype. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics., 159B, 537–548.
Clerx, L., Visser, P. J., Verhey, F., & Aalten, P. (2012). New MRI markers for Alzheimer's disease: A meta-analysis of diffusion tensor imaging and a comparison with medial temporal lobe measurements. Journal of Alzheimer's Disease, 29, 405–429.
Dougherty, D. M., Charles, N. E., Mathias, C. W., Ryan, S. R., Olvera, R. L., Liang, Y., & Acheson, A. (2014). Delay discounting differentiates pre-adolescents at high and low risk for substance use disorders based on family history. Drug and Alcohol Dependence, 143, 105–111.
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., … Thompson, P. M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America, 101, 8174–8179.
Gogtay, N., & Thompson, P. M. (2009). Mapping gray matter development: Implications for typical development and vulnerability to psychopathology. Brain and Cognition, 72, 6–15.
Grech-Sollars, M., Hales, P. W., Miyazaki, K., Raschke, F., Rodriguez, D., Wilson, M., … Clark, C. A. (2015). Multi-centre reproducibility of diffusion MRI parameters for clinical sequences in the brain. NMR in Biomedicine, 28, 468–485.
Hasan, K. M., Iftikhar, A., Kamali, A., Kramer, L. A., Ashtari, M., Cirino, P. T., … Ewing-Cobbs, L. (2009). Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography. Brain Research, 1276, 67–76.
Jahanshad, N., Kochunov, P., Sprooten, E., Mandl, R. C., Nichols, T. E., Almassy, L., … Glahn, D. C. (2013). Multi-site genetic analysis of diffusion images and voxelwise heritability analysis: A pilot project of the ENIGMA-DTI working group. NeuroImage, 81, 455–469. doi:pii: S1053-8119(13)00408-4. 10.1016/j.neuroimage.2013.04.061
Jansen, J. F., Kooi, M. E., Kessels, A. G., Nicolay, K., & Backes, W. H. (2007). Reproducibility of quantitative cerebral T2 relaxometry, diffusion tensor imaging, and 1H magnetic resonance spectroscopy at 3.0 Tesla. Investigative Radiology, 42, 327–337.
Jones, D. K., Horsfield, M. A., & Simmons, A. (1999). Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magnetic Resonance in Medicine, 42, 515–525.
Jovicich, J., Marizzoni, M., Bosch, B., Bartres-Faz, D., Arnold, J., Benninghoff, J., … PharmaCog, C. (2014). Multisite longitudinal reliability of tract-based spatial statistics in diffusion tensor imaging of healthy elderly subjects. NeuroImage, 101, 390–403.
Karlsgodt, K. H., John, M., Ikuta, T., Rigoard, P., Peters, B. D., Derosse, P., … Szeszko, P. R. (2015). The accumbofrontal tract: Diffusion tensor imaging characterization and developmental change from childhood to adulthood. Human Brain Mapping, 36, 4954–4963.
Kochunov, P., Glahn, D. C., Lancaster, J., Thompson, P. M., Kochunov, V., Rogers, B., … Williamson, D. E. (2011). Fractional anisotropy of cerebral white matter and thickness of cortical gray matter across the lifespan. NeuroImage, 58, 41–49.
Kochunov, P., Glahn, D. C., Rowland, L. M., Olvera, R., Wincker, P., Yang, D., … Hong, L. E. (2013). Testing the hypothesis of accelerated cerebral white matter aging in schizophrenia and major depression. Biological Psychiatry, 73, 482–491. doi:10.1016/j.biopsych.2012.10.002
Kochunov, P., Jahanshad, N., Marcus, D., Winkler, A., Sprooten, E., Nichols, T. E., … Van Essen, D. C. (2015). Heritability of fractional anisotropy in human white matter: A comparison of Human Connectome Project and ENIGMA-DTI data. NeuroImage, 111, 300–311.
Kochunov, P., Jahanshad, N., Sprooten, E., Nichols, T. E., Mandl, R. C., Almasy, L., … Glahn, D. C. (2014). Multi-site study of additive genetic effects on fractional anisotropy of cerebral white matter: Comparing meta and megaanalytical approaches for data pooling. NeuroImage, 95C, 136–150.
Kochunov, P. V., Lancaster, J. L., & Fox, P. T. (1999). Accurate high-speed spatial normalization using an octree method. NeuroImage, 10, 724–737.
Kochunov, P., Lancaster, J. L., Glahn, D. C., Purdy, D., Laird, A. R., Gao, F., & Fox, P. (2006). Retrospective motion correction protocol for high-resolution anatomical MRI. Human Brain Mapping, 27, 957–962.
Kochunov, P., Lancaster, J. L., Thompson, P., Woods, R., Mazziotta, J., Hardies, J., & Fox, P. (2001). Regional spatial normalization: Toward an optimal target. Journal of Computer Assisted Tomography, 25, 805–816.
Kochunov, P., Thompson, P. M., Winkler, A., Morrissey, M., Fu, M., Coyle, T. R., … Hong, L. E. (2016). The common genetic influence over processing speed and white matter microstructure: Evidence from the Old Order Amish and Human Connectome Projects. NeuroImage, 125, 189–197.
Kochunov, P., Williamson, D. E., Lancaster, J., Fox, P., Cornell, J., Blangero, J., & Glahn, D. C. (2012). Fractional anisotropy of water diffusion in cerebral white matter across the lifespan. Neurobiology of Aging, 33, 9–20.
Mandl, R. C., Rais, M., van Baal, G. C., van Haren, N. E., Cahn, W., Kahn, R. S., & Hulshoff Pol, H. E. (2012). Altered white matter connectivity in never-medicated patients with schizophrenia. Human Brain Mapping, 34, 2353–2365.
Mori, S., Oishi, K., Jiang, H., Jiang, L., Li, X., Akhter, K., … Mazziotta, J. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage, 40, 570–582.
Rice, J. P., Reich, T., Bucholz, K. K., Neuman, R. J., Fishman, R., Rochberg, N., … Begleiter, H. (1995). Comparison of direct interview and family history diagnoses of alcohol dependence. Alcoholism: Clinical and Experimental Research, 19, 1018–1023.
Ryan, S. R., Acheson, A., Charles, N. E., Lake, S. L., Hernandez, D. L., Mathias, C. W., & Dougherty, D. M. (2016). Clinical and social/environmental characteristics in a community sample of children with and without family histories of substance use disorder in the San Antonio area: A descriptive study. Journal of Child & Adolescent Substance Abuse, 25, 327–339.
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., … Behrens, T. E. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. NeuroImage, 31, 1487–1505.
Smith, S., Jenkinson, M., Woolrich, M., Beckmann, C., Behrens, T., Johansen-Berg, H., … Matthews, P. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23, 208–219.
Sprooten, E., Sussmann, J. E., Clugston, A., Peel, A., McKirdy, J., Moorhead, T. W., … McIntosh, A. M. (2011). White matter integrity in individuals at high genetic risk of bipolar disorder. Biological Psychiatry, 70, 350–356.
Teipel, S., Drzezga, A., Grothe, M. J., Barthel, H., Chetelat, G., Schuff, N., … Fellgiebel, A. (2015). Multimodal imaging in Alzheimer's disease: Validity and usefulness for early detection. The Lancet Neurology, 14, 1037–1053.
Teipel, S. J., Reuter, S., Stieltjes, B., Acosta-Cabronero, J., Ernemann, U., Fellgiebel, A., … Hampel, H. (2011). Multicenter stability of diffusion tensor imaging measures: A European clinical and physical phantom study. Psychiatry Research, 194, 363–371.
Teipel, S. J., Wegrzyn, M., Meindl, T., Frisoni, G., Bokde, A. L., Fellgiebel, A., … Ewers, M. (2012). Anatomical MRI and DTI in the diagnosis of Alzheimer's disease: A European multicenter study. Journal of Alzheimer's Disease, 31, S33–S47.
Vasung, L., Huang, H., Jovanov-Milosevic, N., Pletikos, M., Mori, S., & Kostovic, I. (2010). Development of axonal pathways in the human fetal fronto-limbic brain: Histochemical characterization and diffusion tensor imaging. Journal of Anatomy, 217, 400–417.
Veenith, T. V., Carter, E., Grossac, J., Newcombe, V. F., Outtrim, J. G., Lupson, V., … Coles, J. P. (2013). Inter subject variability and reproducibility of diffusion tensor imaging within and between different imaging sessions. PLoS One, 8, e65941.
Vollmar, C., O'Muircheartaigh, J., Barker, G. J., Symms, M. R., Thompson, P., Kumari, V., … Koepp, M. J. (2010). Identical, but not the same: Intra-site and inter-site reproducibility of fractional anisotropy measures on two 3.0T scanners. NeuroImage, 51, 1384–1394.
Wijtenburg, S. A., McGuire, S. A., Rowland, L. M., Sherman, P. M., Lancaster, J. L., Tate, D. F., … Kochunov, P. (2012). Relationship between fractional anisotropy of cerebral white matter and metabolite concentrations measured using (1)H magnetic resonance spectroscopy in healthy adults. NeuroImage, 66C, 161–168.
