Abstract
Purpose
We aimed to determine the feasibility of using DKI to characterize pathological changes in nonarteritic anterior ischemic optic neuropathy (NAION) and to differentiate it from acute optic neuritis (ON).
Methods
Orbital DKI was performed with a 3.0 T scanner on 75 patients (51 with NAION and 24 with acute ON) and 15 healthy controls. NAION patients were further divided into early and late groups. The mean kurtosis (MK), axial kurtosis (AK), radial kurtosis (RK), mean diffusivity (MD), fractional anisotropy (FA), radial diffusivity (RD), and axial diffusivity (AD) were calculated to perform quantitative analyses among groups; and receiver operating characteristic curve analyses were also performed to determine their effectiveness of differential diagnosis. In addition, correlation coefficients were calculated to explore the correlations of the DKI-derived data with duration of disease.
Results
The MK, RK, and AK in the affected nerves with NAION were significantly higher than those in the controls, while the trend of FA, RD, and AD was a decline; in acute ON patients, except for RD, which increased, all DKI-derived kurtosis and diffusion parameters were significantly lower than controls (all P < 0.008). Only AK and MD had statistical differences between the early and late groups. Except for MD (early group) and FA, all other DKI-derived parameters were higher in NAION than in acute ON; and parameters in the early group showed better diagnostic efficacy in differentiating NAION from acute ON. Correlation analysis showed that time was negatively correlated with MK, RK, AK, and FA and positively correlated with MD, RD, and AD (all P < 0.05).
Conclusion
DKI is helpful for assessing the specific pathologic abnormalities resulting from ischemia in NAION by comparison with acute ON. Early DKI should be performed to aid in the diagnosis and evaluation of NAION.
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Data availability
The authors will supply the relevant data in response to reasonable requests.
References
Biousse V, Newman NJ (2015) Ischemic optic neuropathies. N Engl J Med 372(25):2428–2436. https://doi.org/10.1056/NEJMra1413352
Bernstein SL, Miller NR (2015) Ischemic optic neuropathies and their models: disease comparisons, model strengths and weaknesses. Jpn J Ophthalmol 59(3):135–147. https://doi.org/10.1007/s10384-015-0373-5
Baig MN, Lubow M, Immesoete P, Bergese SD, Hamdy EA, Mendel E (2007) Vision loss after spine surgery: review of the literature and recommendations. Neurosurg Focus 23(5):E15. https://doi.org/10.3171/FOC-07/11/15
Collignon-Robe NJ, Feke GT, Rizzo JF 3rd (2004) Optic nerve head circulation in nonarteritic anterior ischemic optic neuropathy and optic neuritis. Ophthalmology 111(9):1663–1672. https://doi.org/10.1016/j.ophtha.2004.05.020
Khan AA, Hussain SA, Khan M, Corbett JJ (2012) MRI findings of bilateral posterior ischemic optic neuropathy in postcardiac transplant patient. Neurologist 18(5):313–315. https://doi.org/10.1097/NRL.0b013e3182675360
Patel HR, Margo CE (2017) Pathology of ischemic optic neuropathy. Arch Pathol Lab Med 141(1):162–166. https://doi.org/10.5858/arpa.2016-0027-RS
Hattenhauer MG, Leavitt JA, Hodge DO, Grill R, Gray DT (1997) Incidence of nonarteritic anterior ischemic optic neuropathy. Am J Ophthalmol 123(1):103–107
Johnson LN, Arnold AC (1994) Incidence of nonarteritic and arteritic anterior ischemic optic neuropathy. Population-based study in the state of Missouri and Los Angeles County, California. J Neuro-Ophthalmol 14(1):38–44
Duchene G, Peeters F, Peeters A, Duprez T (2017) A comparative study of the sensitivity of diffusion-related parameters obtained from diffusion tensor imaging, diffusional kurtosis imaging, q-space analysis and bi-exponential modelling in the early disease course (24 h) of hyperacute (6 h) ischemic stroke patients. MAGMA 30(4):375–385. https://doi.org/10.1007/s10334-017-0612-5
Federau C, Sumer S, Becce F, Maeder P, O’Brien K, Meuli R, Wintermark M (2014) Intravoxel incoherent motion perfusion imaging in acute stroke: initial clinical experience. Neuroradiology 56(8):629–635. https://doi.org/10.1007/s00234-014-1370-y
Hui ES, Fieremans E, Jensen JH, Tabesh A, Feng W, Bonilha L, Spampinato MV, Adams R, Helpern JA (2012) Stroke assessment with diffusional kurtosis imaging. Stroke 43(11):2968–2973. https://doi.org/10.1161/STROKEAHA.112.657742
Spampinato MV, Chan C, Jensen JH, Helpern JA, Bonilha L, Kautz SA, Nietert PJ, Feng W (2017) Diffusional kurtosis imaging and motor outcome in acute ischemic stroke. AJNR Am J Neuroradiol 38(7):1328–1334. https://doi.org/10.3174/ajnr.A5180
Yin J, Sun H, Wang Z, Ni H, Shen W, Sun PZ (2018) Diffusion kurtosis imaging of acute infarction: comparison with routine diffusion and follow-up MR imaging. Radiology 287(2):651–657. https://doi.org/10.1148/radiol.2017170553
Lu P, Sha Y, Wan H, Wang F, Tian G, Tang W (2017) Assessment of nonarteritic anterior ischemic optic neuropathy with intravoxel incoherent motion diffusion-weighted imaging using readout-segmented echo-planar imaging, parallel imaging, and 2D navigator-based reacquisition. J Magn Reson Imaging : JMRI 46(6):1760–1766. https://doi.org/10.1002/jmri.25760
Mournet S, Sene T, Charbonneau F, Poillon G, Vignal C, Clavel G, Guillaume J, Savatovsky J, Lecler A (2022) Early diffusion-weighted MRI at 3 Tesla detects ischemic changes of the optic nerve in anterior ischemic optic neuropathy. Eur Radiol 32(5):3588–3596. https://doi.org/10.1007/s00330-021-08417-4
Wang MY, Qi PH, Shi DP (2011) Diffusion tensor imaging of the optic nerve in subacute anterior ischemic optic neuropathy at 3T. AJNR Am J Neuroradiol 32(7):1188–1194. https://doi.org/10.3174/ajnr.A2487
Lu P, Yuan T, Liu X, Tian G, Zhang J, Sha Y (2020) Role of diffusional kurtosis imaging in differentiating neuromyelitis optica–related and multiple sclerosis–related acute optic neuritis: comparison with diffusion-weighted imaging. J Comput Assist Tomogr 44(1):47–52. https://doi.org/10.1097/rct.0000000000000974
Hayreh SS, Zimmerman MB (2008) Nonarteritic anterior ischemic optic neuropathy: natural history of visual outcome. Ophthalmology 115(2):298-305 e292. https://doi.org/10.1016/j.ophtha.2007.05.027
Guo YL, Li SJ, Zhang ZP, Shen ZW, Zhang GS, Yan G, Wang YT, Rao HB, Zheng WB, Wu RH (2016) Parameters of diffusional kurtosis imaging for the diagnosis of acute cerebral infarction in different brain regions. Exp Ther Med 12(2):933–938. https://doi.org/10.3892/etm.2016.3390
Lu D, Jiang Y, Ji Y, Zhou IY, Mandeville E, Lo EH, Wang X, Sun PZ (2018) JOURNAL CLUB: Evaluation of diffusion kurtosis imaging of stroke lesion with hemodynamic and metabolic mri in a rodent model of acute stroke. AJR Am J Roentgenol 210(4):720–727. https://doi.org/10.2214/AJR.17.19134
Zhu LH, Zhang ZP, Wang FN, Cheng QH, Guo G (2019) Diffusion kurtosis imaging of microstructural changes in brain tissue affected by acute ischemic stroke in different locations. Neural Regen Res 14(2):272–279. https://doi.org/10.4103/1673-5374.244791
Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K (2005) Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53(6):1432–1440. https://doi.org/10.1002/mrm.20508
Zhang S, Yao Y, Shi J, Tang X, Zhao L, Zhu W (2016) The temporal evolution of diffusional kurtosis imaging in an experimental middle cerebral artery occlusion (MCAO) model. Magn Reson Imaging 34(7):889–895. https://doi.org/10.1016/j.mri.2016.04.016
Jensen JH, Falangola MF, Hu C, Tabesh A, Rapalino O, Lo C, Helpern JA (2011) Preliminary observations of increased diffusional kurtosis in human brain following recent cerebral infarction. NMR Biomed 24(5):452–457. https://doi.org/10.1002/nbm.1610
Yuan L, Sun M, Chen Y, Long M, Zhao X, Yin J, Yan X, Ji D, Ni H (2016) Non-Gaussian diffusion alterations on diffusion kurtosis imaging in patients with early Alzheimer’s disease. Neurosci Lett 616:11–18. https://doi.org/10.1016/j.neulet.2016.01.021
Doring TM, Lopes FCR, Kubo TTA, Tukamoto G, Kimura MC, Strecker RM, Domingues RC, Gasparetto EL (2014) Neuromyelitis optica: a diffusional kurtosis imaging study. Am J Neuroradiol 35(12):2287–2292. https://doi.org/10.3174/ajnr.A4050
Liyan L, Si W, Qian W, Yuhui S, Xiaoer W, Yuehua L, Wenbin L (2017) Diffusion kurtosis as an in vivo imaging marker of early radiation-induced changes in radiation-induced temporal lobe necrosis in nasopharyngeal carcinoma patients. Clin Neuroradiol 28(3):413–420. https://doi.org/10.1007/s00062-017-0585-9
Coutu JP, Chen JJ, Rosas HD, Salat DH (2014) Non-Gaussian water diffusion in aging white matter. Neurobiol Aging 35(6):1412–1421. https://doi.org/10.1016/j.neurobiolaging.2013.12.001
Peters A (2002) The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 31(8–9):581–593
Trip SA, Wheeler-Kingshott C, Jones SJ, Li W-Y, Barker GJ, Thompson AJ, Plant GT, Miller DH (2006) Optic nerve diffusion tensor imaging in optic neuritis. Neuroimage 30(2):498–505. https://doi.org/10.1016/j.neuroimage.2005.09.024
Naismith RT, Xu J, Tutlam NT, Snyder A, Benzinger T, Shimony J, Shepherd J, Trinkaus K, Cross AH, Song SK (2009) Disability in optic neuritis correlates with diffusion tensor-derived directional diffusivities. Neurology 72(7):589–594. https://doi.org/10.1212/01.wnl.0000335766.22758.cd
Yamada I, Kuroiwa T, Endo S, Miyasaka N (2003) Temporal evolution of apparent diffusion coefficient and T2 value following transient focal cerebral ischemia in gerbils. Acta Neurochir Suppl 86:147–151
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Lu, P., Hong, R., Tian, G. et al. Diffusional kurtosis imaging in differentiating nonarteritic anterior ischemic optic neuropathy from acute optic neuritis. Neuroradiology 66, 797–807 (2024). https://doi.org/10.1007/s00234-024-03301-6
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DOI: https://doi.org/10.1007/s00234-024-03301-6