Skip to main content
Top
Published in: Clinical Neuroradiology 3/2018

01-09-2018 | Original Article

Diffusion Kurtosis as an in vivo Imaging Marker of Early Radiation-Induced Changes in Radiation-Induced Temporal Lobe Necrosis in Nasopharyngeal Carcinoma Patients

Authors: Lu Liyan, Wang Si, Wang Qian, Shao Yuhui, Wei Xiaoer, Li Yuehua, Li Wenbin

Published in: Clinical Neuroradiology | Issue 3/2018

Login to get access

Abstract

Purpose

Diffusion kurtosis imaging (DKI), an extension of the popular diffusion tensor imaging (DTI) model, has been applied in clinical studies of brain tissue changes. We explored the value of DKI for the early detection of radiation-induced changes in temporal lobe necrosis (TLN) after radiotherapy (RT) for nasopharyngeal carcinoma (NPC).

Methods

A total of 400 patients with NPC were retrospectively enrolled; all participants underwent MRI scans 0–7 days before RT, at 4 weeks during RT, and 1 month after completing RT. DKI-derived kurtosis parameters (mean kurtosis [MK], axial kurtosis [Ka], radial kurtosis [Kr]), and DKI-derived diffusion parameters (fractional anisotropy [FA], mean diffusivity [MD], axial diffusivity [λa], radial diffusivity [λr]) were assessed in temporal lobe white matter.

Results

Analysis was performed for 20 patients with temporal lobe necrosis following long-term follow-up. No brain abnormalities were visible on conventional MRI in any patient at 4 weeks during RT and 1 month after RT. Of all DKI-derived parameters, MK was significantly lower at 1 month after RT than before RT (P < 0.05).

Conclusion

This study indicates DKI can detect the early presence of relatively subtle RT-induced brain abnormalities before TLN in patients with NPC and may provide a sensitive imaging technique for temporal white matter microstructural abnormalities that are silent on conventional modalities but precede TLN after RT.
Literature
1.
go back to reference Shanmugaratnam K, Chan SH, de-Thé G, Goh JE, Khor TH, Simons MJ, Tye CY. Histopathology of nasopharyngeal carcinoma: correlations with epidemiology, survival rates and other biological characteristics. Cancer. 1979;44:1029–44.CrossRefPubMed Shanmugaratnam K, Chan SH, de-Thé G, Goh JE, Khor TH, Simons MJ, Tye CY. Histopathology of nasopharyngeal carcinoma: correlations with epidemiology, survival rates and other biological characteristics. Cancer. 1979;44:1029–44.CrossRefPubMed
2.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.CrossRefPubMed Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.CrossRefPubMed
3.
go back to reference Zhou GQ, Yu XL, Chen M, Guo R, Lei Y, Sun Y, Mao YP, Liu LZ, Li L, Lin AH, Ma J. Radiation-induced temporal lobe injury for nasopharyngeal carcinoma: a comparison of intensity-modulated radiotherapy and conventional two-dimensional radiotherapy. PLoS One. 2013;8:e67488.CrossRefPubMedPubMedCentral Zhou GQ, Yu XL, Chen M, Guo R, Lei Y, Sun Y, Mao YP, Liu LZ, Li L, Lin AH, Ma J. Radiation-induced temporal lobe injury for nasopharyngeal carcinoma: a comparison of intensity-modulated radiotherapy and conventional two-dimensional radiotherapy. PLoS One. 2013;8:e67488.CrossRefPubMedPubMedCentral
4.
go back to reference Lee AW, Ng SH, Ho JH, Tse VK, Poon YF, Tse CC, Au GK, O SK, Lau WH, Foo WW. Clinical diagnosis of late temporal lobe necrosis following radiation therapy for nasopharyngeal carcinoma. Cancer. 1988;61:1535–42.CrossRefPubMed Lee AW, Ng SH, Ho JH, Tse VK, Poon YF, Tse CC, Au GK, O SK, Lau WH, Foo WW. Clinical diagnosis of late temporal lobe necrosis following radiation therapy for nasopharyngeal carcinoma. Cancer. 1988;61:1535–42.CrossRefPubMed
6.
go back to reference Xiong WF, Qiu SJ, Wang HZ, Lv XF. 1H-MR spectroscopy and diffusion tensor imaging of normal-appearing temporal white matter in patients with nasopharyngeal carcinoma after irradiation: initial experience. J Magn Reson Imaging. 2013;37:101–8.CrossRefPubMed Xiong WF, Qiu SJ, Wang HZ, Lv XF. 1H-MR spectroscopy and diffusion tensor imaging of normal-appearing temporal white matter in patients with nasopharyngeal carcinoma after irradiation: initial experience. J Magn Reson Imaging. 2013;37:101–8.CrossRefPubMed
7.
go back to reference Chapman CH, Nagesh V, Sundgren PC, Buchtel H, Chenevert TL, Junck L, Lawrence TS, Tsien CI, Cao Y. Diffusion tensor imaging of normal-appearing white matter as biomarker for radiation-induced late delayed cognitive decline. Int J Radiat Oncol Biol Phys. 2012;82:2033–40.CrossRefPubMed Chapman CH, Nagesh V, Sundgren PC, Buchtel H, Chenevert TL, Junck L, Lawrence TS, Tsien CI, Cao Y. Diffusion tensor imaging of normal-appearing white matter as biomarker for radiation-induced late delayed cognitive decline. Int J Radiat Oncol Biol Phys. 2012;82:2033–40.CrossRefPubMed
8.
go back to reference Wang HZ, Qiu SJ, Lv XF, Wang YY, Liang Y, Xiong WF, Ouyang ZB. Diffusion tensor imaging and 1H-MRS study on radiation-induced brain injury after nasopharyngeal carcinoma radiotherapy. Clin Radiol. 2012;67:340–5.CrossRefPubMed Wang HZ, Qiu SJ, Lv XF, Wang YY, Liang Y, Xiong WF, Ouyang ZB. Diffusion tensor imaging and 1H-MRS study on radiation-induced brain injury after nasopharyngeal carcinoma radiotherapy. Clin Radiol. 2012;67:340–5.CrossRefPubMed
9.
go back to reference Basser PJ, Jones DK. Diffusion-tensor MRI: theory, experimental design and data analysis – a technical review. NMR Biomed. 2002;15:456–67.CrossRefPubMed Basser PJ, Jones DK. Diffusion-tensor MRI: theory, experimental design and data analysis – a technical review. NMR Biomed. 2002;15:456–67.CrossRefPubMed
10.
go back to reference Tuch DS, Reese TG, Wiegell MR, Wedeen VJ. Diffusion MRI of complex neural architecture. Neuron. 2003;40:885–95.CrossRefPubMed Tuch DS, Reese TG, Wiegell MR, Wedeen VJ. Diffusion MRI of complex neural architecture. Neuron. 2003;40:885–95.CrossRefPubMed
11.
go back to reference Winston GP. The potential role of novel diffusion imaging techniques in the understanding and treatment of epilepsy. Quant Imaging Med Surg. 2015;5:279–87.PubMedPubMedCentral Winston GP. The potential role of novel diffusion imaging techniques in the understanding and treatment of epilepsy. Quant Imaging Med Surg. 2015;5:279–87.PubMedPubMedCentral
12.
go back to reference Zhu J, Zhuo C, Qin W, Wang D, Ma X, Zhou Y, Yu C. Performances of diffusion kurtosis imaging and diffusion tensor imaging in detecting white matter abnormality in schizophrenia. Neuroimage Clin. 2015;7:170–6.CrossRefPubMed Zhu J, Zhuo C, Qin W, Wang D, Ma X, Zhou Y, Yu C. Performances of diffusion kurtosis imaging and diffusion tensor imaging in detecting white matter abnormality in schizophrenia. Neuroimage Clin. 2015;7:170–6.CrossRefPubMed
13.
go back to reference Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med. 2005;53:1432–40.CrossRefPubMed Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med. 2005;53:1432–40.CrossRefPubMed
15.
go back to reference Lu H, Jensen JH, Ramani A, Helpern JA. Three-dimensional characterization of non-gaussian water diffusion in humans using diffusion kurtosis imaging. NMR Biomed. 2006;19:236–47.CrossRefPubMed Lu H, Jensen JH, Ramani A, Helpern JA. Three-dimensional characterization of non-gaussian water diffusion in humans using diffusion kurtosis imaging. NMR Biomed. 2006;19:236–47.CrossRefPubMed
16.
go back to reference Falangola MF, Jensen JH, Babb JS, Hu C, Castellanos FX, Di Martino A, Ferris SH, Helpern JA. Age-related Non-Gaussian diffusion patterns in the prefrontal brain. J Magn Reson Imaging. 2008;28:1345–50.CrossRefPubMedPubMedCentral Falangola MF, Jensen JH, Babb JS, Hu C, Castellanos FX, Di Martino A, Ferris SH, Helpern JA. Age-related Non-Gaussian diffusion patterns in the prefrontal brain. J Magn Reson Imaging. 2008;28:1345–50.CrossRefPubMedPubMedCentral
17.
go back to reference Helpern JA, Adisetiyo V, Falangola MF, Hu C, Di Martino A, Williams K, Castellanos FX, Jensen JH. Preliminary evidence of altered gray and white matter microstructural development in the frontal lobe of adolescents with attention-deficit hyperactivity disorder: a diffusional kurtosis imaging study. J Magn Reson Imaging. 2011;33:17–23.CrossRefPubMedPubMedCentral Helpern JA, Adisetiyo V, Falangola MF, Hu C, Di Martino A, Williams K, Castellanos FX, Jensen JH. Preliminary evidence of altered gray and white matter microstructural development in the frontal lobe of adolescents with attention-deficit hyperactivity disorder: a diffusional kurtosis imaging study. J Magn Reson Imaging. 2011;33:17–23.CrossRefPubMedPubMedCentral
18.
go back to reference Raab P, Hattingen E, Franz K, Zanella FE, Lanfermann H. Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. Radiology. 2010;254:876–81.CrossRefPubMed Raab P, Hattingen E, Franz K, Zanella FE, Lanfermann H. Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. Radiology. 2010;254:876–81.CrossRefPubMed
19.
go back to reference Zhang Y, Yan X, Gao Y, Xu D, Wu J, Li Y. A preliminary study of epilepsy in children using diffusional kurtosis imaging. Clin Neuroradiol. 2013;23:293–300.CrossRefPubMed Zhang Y, Yan X, Gao Y, Xu D, Wu J, Li Y. A preliminary study of epilepsy in children using diffusional kurtosis imaging. Clin Neuroradiol. 2013;23:293–300.CrossRefPubMed
20.
go back to reference Gao Y, Zhang Y, Wong CS, Wu PM, Zhang Z, Gao J, Qiu D, Huang B. Diffusion abnormalities in temporal lobes of children with temporal lobe epilepsy: a preliminary diffusional kurtosis imaging study and comparison with diffusion tensor imaging. NMR Biomed. 2012;25:1369–77.CrossRefPubMed Gao Y, Zhang Y, Wong CS, Wu PM, Zhang Z, Gao J, Qiu D, Huang B. Diffusion abnormalities in temporal lobes of children with temporal lobe epilepsy: a preliminary diffusional kurtosis imaging study and comparison with diffusion tensor imaging. NMR Biomed. 2012;25:1369–77.CrossRefPubMed
21.
go back to reference Jansen JF, Stambuk HE, Koutcher JA, Shukla-Dave A. Non-Gaussian analysis of diffusion-weighted MR imaging in head and neck squamous cell carcinoma: a feasibility study. AJNR Am J Neuroradiol. 2010;31:741–8.CrossRefPubMed Jansen JF, Stambuk HE, Koutcher JA, Shukla-Dave A. Non-Gaussian analysis of diffusion-weighted MR imaging in head and neck squamous cell carcinoma: a feasibility study. AJNR Am J Neuroradiol. 2010;31:741–8.CrossRefPubMed
22.
go back to reference Cheung MM, Hui ES, Chan KC, Helpern JA, Qi L, Wu EX. Does diffusion kurtosis imaging lead to better neural tissue characterization? A rodent brain maturation study. Neuroimage. 2009;45:386–92.CrossRefPubMed Cheung MM, Hui ES, Chan KC, Helpern JA, Qi L, Wu EX. Does diffusion kurtosis imaging lead to better neural tissue characterization? A rodent brain maturation study. Neuroimage. 2009;45:386–92.CrossRefPubMed
23.
go back to reference Tabesh A, Jensen JH, Ardekani BA, Helpern JA. Estimation of tensors and tensor-derived measures in diffusional kurtosis imaging. Magn Reson Med. 2011;65:823–36.CrossRefPubMed Tabesh A, Jensen JH, Ardekani BA, Helpern JA. Estimation of tensors and tensor-derived measures in diffusional kurtosis imaging. Magn Reson Med. 2011;65:823–36.CrossRefPubMed
24.
go back to reference Wang D, Li YH, Fu J, Wang H. Diffusion kurtosis imaging study on temporal lobe after nasopharyngeal carcinoma radiotherapy. Brain Res. 2016;1648:387–93.CrossRefPubMed Wang D, Li YH, Fu J, Wang H. Diffusion kurtosis imaging study on temporal lobe after nasopharyngeal carcinoma radiotherapy. Brain Res. 2016;1648:387–93.CrossRefPubMed
25.
go back to reference Stokum JA, Sours C, Zhuo J, Kane R, Shanmuganathan K, Gullapalli RP. A longitudinal evaluation of diffusion kurtosis imaging in patients with mild traumatic brain injury. Brain Inj. 2015;29:47–57.CrossRefPubMed Stokum JA, Sours C, Zhuo J, Kane R, Shanmuganathan K, Gullapalli RP. A longitudinal evaluation of diffusion kurtosis imaging in patients with mild traumatic brain injury. Brain Inj. 2015;29:47–57.CrossRefPubMed
26.
go back to reference Kamagata K, Tomiyama H, Motoi Y, Kano M, Abe O, Ito K, Shimoji K, Suzuki M, Hori M, Nakanishi A, Kuwatsuru R, Sasai K, Aoki S, Hattori N. Diffusional kurtosis imaging of cingulate fibers in Parkinson disease: comparison with conventional diffusion tensor imaging. Magn Reson Imaging. 2013;31:1501–6.CrossRefPubMed Kamagata K, Tomiyama H, Motoi Y, Kano M, Abe O, Ito K, Shimoji K, Suzuki M, Hori M, Nakanishi A, Kuwatsuru R, Sasai K, Aoki S, Hattori N. Diffusional kurtosis imaging of cingulate fibers in Parkinson disease: comparison with conventional diffusion tensor imaging. Magn Reson Imaging. 2013;31:1501–6.CrossRefPubMed
27.
go back to reference Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002;17:1429–36.CrossRefPubMed Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002;17:1429–36.CrossRefPubMed
28.
go back to reference Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003;20:1714–22.CrossRefPubMed Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003;20:1714–22.CrossRefPubMed
29.
go back to reference Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage. 2005;26:132–40.CrossRefPubMed Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage. 2005;26:132–40.CrossRefPubMed
30.
go back to reference Harsan LA, Poulet P, Guignard B, Steibel J, Parizel N, de Sousa PL, Boehm N, Grucker D, Ghandour MS. Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. J Neurosci Res. 2006;83:392–402.CrossRefPubMed Harsan LA, Poulet P, Guignard B, Steibel J, Parizel N, de Sousa PL, Boehm N, Grucker D, Ghandour MS. Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. J Neurosci Res. 2006;83:392–402.CrossRefPubMed
31.
go back to reference Ono J, Harada K, Takahashi M, Maeda M, Ikenaka K, Sakurai K, Sakai N, Kagawa T, Fritz-Zieroth B, Nagai T. Differentiation between dysmyelination and demyelination using magnetic resonance diffusional anisotropy. Brain Res. 1995;671:141–8.CrossRefPubMed Ono J, Harada K, Takahashi M, Maeda M, Ikenaka K, Sakurai K, Sakai N, Kagawa T, Fritz-Zieroth B, Nagai T. Differentiation between dysmyelination and demyelination using magnetic resonance diffusional anisotropy. Brain Res. 1995;671:141–8.CrossRefPubMed
32.
go back to reference Lee CY, Tabesh A, Spampinato MV, Helpern JA, Jensen JH, Bonilha L. Diffusional kurtosis imaging reveals a distinctive pattern of microstructural alternations in idiopathic generalized epilepsy. Acta Neurol Scand. 2014;130:148–55.CrossRefPubMedPubMedCentral Lee CY, Tabesh A, Spampinato MV, Helpern JA, Jensen JH, Bonilha L. Diffusional kurtosis imaging reveals a distinctive pattern of microstructural alternations in idiopathic generalized epilepsy. Acta Neurol Scand. 2014;130:148–55.CrossRefPubMedPubMedCentral
33.
34.
go back to reference Lee CY, Bennett KM, Debbins JP. Sensitivities of statistical distribution model and diffusion kurtosis model in varying microstructural environments: a Monte Carlo study. J Magn Reson. 2013;230:19–26.CrossRefPubMed Lee CY, Bennett KM, Debbins JP. Sensitivities of statistical distribution model and diffusion kurtosis model in varying microstructural environments: a Monte Carlo study. J Magn Reson. 2013;230:19–26.CrossRefPubMed
35.
go back to reference Coutu JP, Chen JJ, Rosas HD, Salat DH. Non-Gaussian water diffusion in aging white matter. Neurobiol Aging. 2014;35:1412–21.CrossRefPubMed Coutu JP, Chen JJ, Rosas HD, Salat DH. Non-Gaussian water diffusion in aging white matter. Neurobiol Aging. 2014;35:1412–21.CrossRefPubMed
36.
go back to reference Bartzokis G. Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease. Neurobiol Aging. 2004;25:5–18.CrossRefPubMed Bartzokis G. Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease. Neurobiol Aging. 2004;25:5–18.CrossRefPubMed
37.
go back to reference Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H. Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology. 1993;43:1683–9.CrossRefPubMed Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H. Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology. 1993;43:1683–9.CrossRefPubMed
38.
go back to reference Peters A. The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol. 2002;31:581–93.CrossRefPubMed Peters A. The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol. 2002;31:581–93.CrossRefPubMed
Metadata
Title
Diffusion Kurtosis as an in vivo Imaging Marker of Early Radiation-Induced Changes in Radiation-Induced Temporal Lobe Necrosis in Nasopharyngeal Carcinoma Patients
Authors
Lu Liyan
Wang Si
Wang Qian
Shao Yuhui
Wei Xiaoer
Li Yuehua
Li Wenbin
Publication date
01-09-2018
Publisher
Springer Berlin Heidelberg
Published in
Clinical Neuroradiology / Issue 3/2018
Print ISSN: 1869-1439
Electronic ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-017-0585-9

Other articles of this Issue 3/2018

Clinical Neuroradiology 3/2018 Go to the issue