Influence of analytic techniques on comparing DTI-derived measurements in early stage Parkinson's disease

Virendra R Mishra, Karthik R Sreenivasan, Xiaowei Zhuang, Zhengshi Yang, Dietmar Cordes, Ryan R Walsh, Virendra R Mishra, Karthik R Sreenivasan, Xiaowei Zhuang, Zhengshi Yang, Dietmar Cordes, Ryan R Walsh

Abstract

Diffusion tensor imaging (DTI) studies in early Parkinson's disease (PD) to understand pathologic changes in white matter (WM) organization are variable in their findings. Evaluation of different analytic techniques frequently employed to understand the DTI-derived change in WM organization in a multisite, well-characterized, early stage PD cohort should aid the identification of the most robust analytic techniques to be used to investigate WM pathology in this disease, an important unmet need in the field. Thus, region of interest (ROI)-based analysis, voxel-based morphometry (VBM) analysis with varying spatial smoothing, and the two most widely used skeletonwise approaches (tract-based spatial statistics, TBSS, and tensor-based registration, DTI-TK) were evaluated in a DTI dataset of early PD and Healthy Controls (HC) from the Parkinson's Progression Markers Initiative (PPMI) cohort. Statistical tests on the DTI-derived metrics were conducted using a nonparametric approach from this cohort of early PD, after rigorously controlling for motion and signal artifacts during DTI scan which are frequent confounds in this disease population. Both TBSS and DTI-TK revealed a significantly negative correlation of fractional anisotropy (FA) with disease duration. However, only DTI-TK revealed radial diffusivity (RD) to be driving this FA correlation with disease duration. HC had a significantly positive correlation of MD with cumulative DaT score in the right middle-frontal cortex after a minimum smoothing level (at least 13mm) was attained. The present study found that scalar DTI-derived measures such as FA, MD, and RD should be used as imaging biomarkers with caution in early PD as the conclusions derived from them are heavily dependent on the choice of the analysis used. This study further demonstrated DTI-TK may be used to understand changes in DTI-derived measures with disease progression as it was found to be more accurate than TBSS. In addition, no singular region was identified that could explain both disease duration and severity in early PD. The results of this study should help standardize the utilization of DTI-derived measures in PD in an effort to improve comparability across studies and time, and to minimize variability in reported results due to variation in techniques.

Keywords: Neuroscience.

Figures

Fig. 1
Fig. 1
Skeletonwise results of WM organization in PD. The location of the cluster showing a significantly (pcorr<0.05) negative relationship between FA and disease duration using both TBSS (a) and DTI-TK (b). The top and bottom panel of (b) shows the location of the cluster showing a significantly (pcorr<0.05) negative and positive relationship between FA (top panel) and RD (bottom panel), and disease duration using DTI-TK. R and L represent the right and left hemispheres respectively. Color bar represents the range of p-values in the overlaid cluster.
Fig. 2
Fig. 2
VBM-based results of the effect of smoothing before statistical analysis. (a) Top panel: Location of the cluster, involving right middle frontal gyrus, where MD in HC was significantly (pcorr<0.05) correlated with DaT score. Bottom panel: Scatterplot of the extent of the cluster and p-values as a function of spatial smoothing (left panel), along with scatterplot of the extent of the cluster and effect size as a function of spatial smoothing (right panel) is shown. R and L represent the right and left hemispheres respectively.

References

    1. Aarsland D., Creese B., Politis M., Chaudhuri K.R., Ffytche D.H., Weintraub D., Ballard C. Cognitive decline in Parkinson disease. Nat. Rev. Neurol. 2017;13:217–231.
    1. Acosta-Cabronero J., Alley S., Williams G.B., Pengas G., Nestor P.J. Diffusion tensor metrics as biomarkers in alzheimer's disease. PLoS One. 2012;7
    1. Alexander G.E. Biology of Parkinson’s disease: pathogenesis and pathophysiology of a multisystem neurodegenerative disorder. Dialogues Clin. Neurosci. 2004;6:259–280.
    1. Atkinson-Clement C., Pinto S., Eusebio A., Coulon O. Diffusion tensor imaging in Parkinson’s disease: review and meta-analysis. NeuroImage Clin. 2017;16:98–110.
    1. Aung W.Y., Mar S., Benzinger T.L.S. Diffusion tensor MRI as a biomarker in axonal and myelin damage. Imaging Med. 2013;5:427–440.
    1. Bach M., Laun F.B., Leemans A., Tax C.M.W., Biessels G.J., Stieltjes B., Maier-Hein K.H. Methodological considerations on tract-based spatial statistics (TBSS) Neuroimage. 2014;100:358–369.
    1. Borghammer P., Ostergaard K., Cumming P., Gjedde A., Rodell A., Hall N., Chakravarty M.M. A deformation-based morphometry study of patients with early-stage Parkinson’s disease. Eur. J. Neurol. 2010;17:314–320.
    1. Brooks D.J. Imaging approaches to Parkinson disease. J. Nucl. Med. 2010;51:596–609.
    1. Burciu R.G., Ofori E., Archer D.B., Wu S.S., Pasternak O., McFarland N.R., Okun M.S., Vaillancourt D.E. Progression marker of Parkinson’s disease: a 4-year multi-site imaging study. Brain. 2017;140:2183–2192.
    1. Cabeen R.P., Bastin M.E., Laidlaw D.H. A comparative evaluation of voxel-based spatial mapping in diffusion tensor imaging. Neuroimage. 2017;146:100–112.
    1. Cochrane C.J., Ebmeier K.P. Diffusion tensor imaging in parkinsonian syndromes: a systematic review and meta-analysis. Neurology. 2013;80:857–864.
    1. Cordes D., Zhuang X., Kaleem M., Sreenivasan K., Yang Z., Mishra V., Banks S.J., Bluett B., Cummings J.L. Advances in functional magnetic resonance imaging data analysis methods using Empirical Mode Decomposition to investigate temporal changes in early Parkinson’s disease. Alzheimer's Dement. Transl. Res. Clin. Interv. 2018
    1. Díez-Cirarda M., Strafella A.P., Kim J., Peña J., Ojeda N., Cabrera-Zubizarreta A., Ibarretxe-Bilbao N. Dynamic functional connectivity in Parkinson’s disease patients with mild cognitive impairment and normal cognition. NeuroImage Clin. 2018;17:847–855.
    1. Eidelberg D. Oxford University Press; New York, NY: 2011. Imaging in Parkinson’s Disease.
    1. Fioravanti V., Benuzzi F., Codeluppi L., Contardi S., Cavallieri F., Nichelli P., Valzania F. MRI correlates of Parkinson’s disease progression: a voxel based morphometry study. Parkinsons. Dis. 2015;2015:378032.
    1. Fortin J.-P., Parker D., Tunc B., Watanabe T., Elliott M.A., Ruparel K., Roalf D.R., Satterthwaite T.D., Gur R.C., Gur R.E., Schultz R.T., Verma R., Shinohara R.T. Harmonization of multi-site diffusion tensor imaging data. Neuroimage. 2017;161:149–170.
    1. Goedert M., Spillantini M.G., Del Tredici K., Braak H. 100 years of Lewy pathology. Nat. Rev. Neurol. 2013;9:13–24.
    1. Hawkes C.H., Del Tredici K., Braak H. A timeline for Parkinson’s disease. Park. Relat. Disord. 2010;16:79–84.
    1. Hirata F.C.C., Sato J.R., Vieira G., Lucato L.T., Leite C.C., Bor-Seng-Shu E., Pastorello B.F., Otaduy M.C.G., Chaim K.T., Campanholo K.R., Novaes N.P., Melo L.M., Gonçalves M.R., do Nascimento F.B.P., Teixeira M.J., Barbosa E.R., Amaro E., Cardoso E.F. Substantia nigra fractional anisotropy is not a diagnostic biomarker of Parkinson’s disease: a diagnostic performance study and meta-analysis. Eur. Radiol. 2017;27:2640–2648.
    1. Holroyd S., Wooten G.F. Preliminary FMRI evidence of visual system dysfunction in Parkinson’s disease patients with visual hallucinations. J. Neuropsychiatry Clin. Neurosci. 2006;18:402–404.
    1. Hotelling H. The generalization of student’s ratio. Ann. Math. Stat. 1931;2:360–378.
    1. Hua K., Zhang J., Wakana S., Jiang H., Li X., Reich D.S., Calabresi P.A., Pekar J.J., van Zijl P.C.M., Mori S. Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage. 2008;39:336–347.
    1. Jones D.K., Symms M.R., Cercignani M., Howard R.J. The effect of filter size on VBM analyses of DT-MRI data. Neuroimage. 2005;26:546–554.
    1. Kaji Y., Hirata K. Apathy and anhedonia in Parkinson’s disease. ISRN Neurol. 2011;2011:219427.
    1. Kamagata K., Tomiyama H., Hatano T., Motoi Y., Abe O., Shimoji K., Kamiya K., Suzuki M., Hori M., Yoshida M., Hattori N., Aoki S. A preliminary diffusional kurtosis imaging study of Parkinson disease: comparison with conventional diffusion tensor imaging. Neuroradiology. 2014;56:251–258.
    1. Karagulle Kendi A.T., Lehericy S., Luciana M., Ugurbil K., Tuite P. Altered diffusion in the frontal lobe in Parkinson disease. AJNR. Am. J. Neuroradiol. 2008;29:501–505.
    1. Keuken M.C., Bazin P.-L., Crown L., Hootsmans J., Laufer A., Muller-Axt C., Sier R., van der Putten E.J., Schafer A., Turner R., Forstmann B.U. Quantifying inter-individual anatomical variability in the subcortex using 7 T structural MRI. Neuroimage. 2014;94:40–46.
    1. Krajcovicova L., Mikl M., Marecek R., Rektorova I. The default mode network integrity in patients with Parkinson’s disease is levodopa equivalent dose-dependent. J. Neural Transm. 2012;119:443–454.
    1. Kudlicka A., Clare L., Hindle J.V. Executive functions in Parkinson’s disease: systematic review and meta-analysis. Mov. Disord. 2011;26:2305–2315.
    1. Lang A.E., Mikulis D. A new sensitive imaging biomarker for Parkinson disease? Neurology. 2009;72:1374–1375.
    1. Langley J., Huddleston D.E., Merritt M., Chen X., McMurray R., Silver M., Factor S.A., Hu X. Diffusion tensor imaging of the substantia nigra in Parkinson’s disease revisited. Hum. Brain Mapp. 2016;37:2547–2556.
    1. Lee J.E., Chung M.K., Lazar M., DuBray M.B., Kim J., Bigler E.D., Lainhart J.E., Alexander A.L. A study of diffusion tensor imaging by tissue-specific, smoothing-compensated voxel-based analysis. Neuroimage. 2009;44:870–883.
    1. Leemans A., Jones D.K. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn. Reson. Med. 2009;61:1336–1349.
    1. Lehericy S., Vaillancourt D.E., Seppi K., Monchi O., Rektorova I., Antonini A., McKeown M.J., Masellis M., Berg D., Rowe J.B., Lewis S.J.G., Williams-Gray C.H., Tessitore A., Siebner H.R. The role of high-field magnetic resonance imaging in parkinsonian disorders: pushing the boundaries forward. Mov. Disord. 2017;32:510–525.
    1. Lenfeldt N., Larsson A., Nyberg L., Birgander R., Forsgren L. Fractional anisotropy in the substantia nigra in Parkinson’s disease: a complex picture. Eur. J. Neurol. 2015;22:1408–1414.
    1. Magrinelli F., Picelli A., Tocco P., Federico A., Roncari L., Smania N., Zanette G., Tamburin S. Pathophysiology of motor dysfunction in Parkinson’s disease as the rationale for drug treatment and rehabilitation. Parkinsons. Dis. 2016;2016:9832839.
    1. Marsh L. Depression and Parkinson’s disease: current knowledge. Curr. Neurol. Neurosci. Rep. 2013;13:409.
    1. Meireles J., Massano J. Cognitive impairment and dementia in Parkinson’s disease: clinical features, diagnosis, and management. Front. Neurol. 2012
    1. Menke R.A., Jbabdi S., Miller K.L., Matthews P.M., Zarei M. Connectivity-based segmentation of the substantia nigra in human and its implications in Parkinson’s disease. Neuroimage. 2010;52:1175–1180.
    1. Meszlényi R.J., Hermann P., Buza K., Gál V., Vidnyánszky Z. Resting state fMRI functional connectivity analysis using dynamic time warping. Front. Neurosci. 2017;11:75.
    1. Mishra V., Guo X., Delgado M.R., Huang H. Towards tract-specific fractional anisotropy (TSFA) at crossing-fiber regions with clinical diffusion MRI. Magn. Reson. Med. 2015;74:1768–1779.
    1. Mishra V.R., Zhuang X., Sreenivasan K.R., Banks S.J., Yang Z., Bernick C., Cordes D. Multimodal MR imaging signatures of cognitive impairment in active professional fighters. Radiology. 2017;162403
    1. Mori S., Tournier J.-D. second ed. Academic Press; Oxford, UK: 2014. Introduction to Diffusion Tensor Imaging and Higher Order Models.
    1. Murty V.P., Shermohammed M., Smith D.V., Carter R.M., Huettel S.A., Adcock R.A. Resting state networks distinguish human ventral tegmental area from substantia nigra. Neuroimage. 2014;100:580–589.
    1. Nakamura K., Sugaya K. Neuromelanin-sensitive magnetic resonance imaging: a promising technique for depicting tissue characteristics containing neuromelanin. Neural Regen. Res. 2014;9:759–760.
    1. Planetta P.J., Ofori E., Pasternak O., Burciu R.G., Shukla P., DeSimone J.C., Okun M.S., McFarland N.R., Vaillancourt D.E. Free-water imaging in Parkinson’s disease and atypical parkinsonism. Brain. 2016;139:495–508.
    1. Politis M. Neuroimaging in Parkinson disease: from research setting to clinical practice. Nat. Rev. Neurol. 2014;10:708–722.
    1. Pozorski V., Oh J.M., Adluru N., Merluzzi A.P., Theisen F., Okonkwo O., Barzgari A., Krislov S., Sojkova J., Bendlin B.B., Johnson S.C., Alexander A.L., Gallagher C.L. Longitudinal white matter microstructural change in Parkinson’s disease. Hum. Brain Mapp. 2018;39:4150–4161.
    1. PPMI The Parkinson progression marker initiative (PPMI) Prog. Neurobiol. 2011;95:629–635.
    1. Prodoehl J., Burciu R.G., Vaillancourt D.E. Resting state functional magnetic resonance imaging in Parkinson’s disease. Curr. Neurol. Neurosci. Rep. 2014;14:448.
    1. Rae C.L., Correia M.M., Altena E., Hughes L.E., Barker R.A., Rowe J.B. White matter pathology in Parkinson’s disease: the effect of imaging protocol differences and relevance to executive function. Neuroimage. 2012
    1. Rolinski M., Griffanti L., Szewczyk-Krolikowski K., Menke R.A.L., Wilcock G.K., Filippini N., Zamboni G., Hu M.T.M., Mackay C.E. Aberrant functional connectivity within the basal ganglia of patients with Parkinson’s disease. NeuroImage. Clin. 2015;8:126–132.
    1. Schwarz S.T., Abaei M., Gontu V., Morgan P.S., Bajaj N., Auer D.P. Diffusion tensor imaging of nigral degeneration in Parkinson’s disease: a region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. NeuroImage. Clin. 2013;3:481–488.
    1. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2009;44:83–98.
    1. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E.J. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006;31:1487–1505.
    1. Sulzer D., Cassidy C., Horga G., Kang U.J., Fahn S., Casella L., Pezzoli G., Langley J., Hu X.P., Zucca F.A., Isaias I.U., Zecca L. Neuromelanin detection by magnetic resonance imaging (MRI) and its promise as a biomarker for Parkinson’s disease. npj Park. Dis. 2018;4:11.
    1. Tessitore A., Esposito F., Vitale C., Santangelo G., Amboni M., Russo A., Corbo D., Cirillo G., Barone P., Tedeschi G. Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease. Neurology. 2012;79:2226–2232.
    1. Tessitore A., Giordano A., De Micco R., Russo A., Tedeschi G. Sensorimotor connectivity in Parkinson’s disease: the role of functional neuroimaging. Front. Neurol. 2014;5:180.
    1. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15:273–289.
    1. Vaillancourt D.E., Spraker M.B., Prodoehl J., Abraham I., Corcos D.M., Zhou X.J., Comella C.L., Little D.M. High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology. 2009;72:1378–1384.
    1. Walsh R.R. Functional imaging markers as outcome measures in clinical trials for Parkinson’s disease. In: Espay A.J., Fernandez H.H., Fox S.H., Galvez-Jimenez N., editors. Parkinson’s Disease: Current & Future Therapeutics & Clinical Trials. Cambridge University Press; 2016.
    1. Watson G.S., Leverenz J.B. Profile of cognitive impairment in Parkinson disease. Brain Pathol. 2010;20:640–645.
    1. Wen M.-C., Heng H.S.E., Ng S.Y.E., Tan L.C.S., Chan L.L., Tan E.K. White matter microstructural characteristics in newly diagnosed Parkinson’s disease: an unbiased whole-brain study. Sci. Rep. 2016;6:35601.
    1. Winkler A.M., Ridgway G.R., Webster M.A., Smith S.M., Nichols T.E. Permutation inference for the general linear model. Neuroimage. 2014;92:381–397.
    1. Yarnall A.J., Rochester L., Burn D.J. Mild cognitive impairment in Parkinson’s disease. Age Ageing. 2013;42:567–576.
    1. Zeighami Y., Ulla M., Iturria-Medina Y., Dadar M., Zhang Y., Larcher K.M.-H., Fonov V., Evans A.C., Collins D.L., Dagher A. Network structure of brain atrophy in de novo Parkinson’s disease. Elife. 2015;4
    1. Zhang H., Yushkevich P.A., Alexander D.C., Gee J.C. Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 2006;10:764–785.
    1. Zhang K., Yu C., Zhang Y., Wu X., Zhu C., Chan P., Li K. Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson’s disease. Eur. J. Radiol. 2011;77:269–273.
    1. Zhuang X., Walsh R.R., Sreenivasan K.R., Yang Z., Mishra V.R., Cordes D. Exploring the dynamics of resting-state networks in Parkinson’s Disease using Co-Activation Pattern. Neuroimage. 2018

Source: PubMed

3
Subskrybuj