Skip to main content
Erschienen in: Neuroradiology 12/2016

29.10.2016 | Functional Neuroradiology

Assessment of tissue heterogeneity using diffusion tensor and diffusion kurtosis imaging for grading gliomas

verfasst von: Rajikha Raja, Neelam Sinha, Jitender Saini, Anita Mahadevan, KVL Narasinga Rao, Aarthi Swaminathan

Erschienen in: Neuroradiology | Ausgabe 12/2016

Einloggen, um Zugang zu erhalten

Abstract

Introduction

In this work, we aim to assess the significance of diffusion tensor imaging (DTI) and diffusion kurtosis imaging (DKI) parameters in grading gliomas.

Methods

Retrospective studies were performed on 53 subjects with gliomas belonging to WHO grade II (n = 19), grade III (n = 20) and grade IV (n = 14). Expert marked regions of interest (ROIs) covering the tumour on T2-weighted images. Statistical texture measures such as entropy and busyness calculated over ROIs on diffusion parametric maps were used to assess the tumour heterogeneity. Additionally, we propose a volume heterogeneity index derived from cross correlation (CC) analysis as a tool for grading gliomas. The texture measures were compared between grades by performing the Mann-Whitney test followed by receiver operating characteristic (ROC) analysis for evaluating diagnostic accuracy.

Results

Entropy, busyness and volume heterogeneity index for all diffusion parameters except fractional anisotropy and anisotropy of kurtosis showed significant differences between grades. The Mann-Whitney test on mean diffusivity (MD), among DTI parameters, resulted in the highest discriminability with values of P = 0.029 (0.0421) for grade II vs. III and P = 0.0312 (0.0415) for III vs. IV for entropy (busyness). In DKI, mean kurtosis (MK) showed the highest discriminability, P = 0.018 (0.038) for grade II vs. III and P = 0.022 (0.04) for III vs. IV for entropy (busyness). Results of CC analysis illustrate the existence of homogeneity in volume (uniformity across slices) for lower grades, as compared to higher grades. Hypothesis testing performed on volume heterogeneity index showed P values of 0.0002 (0.0001) and 0.0003 (0.0003) between grades II vs. III and III vs. IV, respectively, for MD (MK).

Conclusion

In summary, the studies demonstrated great potential towards automating grading gliomas by employing tumour heterogeneity measures on DTI and DKI parameters.
Literatur
1.
Zurück zum Zitat Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Paul Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97–109CrossRefPubMedPubMedCentral Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Paul Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97–109CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Van Cauter S, De Keyzer F, Sima DM, Sava AC, D’Arco F, Veraart J, Peeters RR, Leemans A, Van Gool S, Wilms G, Demaerel P (2014) Integrating diffusion kurtosis imaging, dynamic susceptibility-weighted contrast-enhanced MRI, and short echo time chemical shift imaging for grading gliomas. Neuro-Oncology 16(7):1010–1021CrossRefPubMedPubMedCentral Van Cauter S, De Keyzer F, Sima DM, Sava AC, D’Arco F, Veraart J, Peeters RR, Leemans A, Van Gool S, Wilms G, Demaerel P (2014) Integrating diffusion kurtosis imaging, dynamic susceptibility-weighted contrast-enhanced MRI, and short echo time chemical shift imaging for grading gliomas. Neuro-Oncology 16(7):1010–1021CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Inoue T, Ogasawara K, Beppu T, Ogawa A, Kabasawa H (2005) Diffusion tensor imaging for preoperative evaluation of tumor grade in gliomas. Clin Neurol Neurosurg 107(3):174–180CrossRefPubMed Inoue T, Ogasawara K, Beppu T, Ogawa A, Kabasawa H (2005) Diffusion tensor imaging for preoperative evaluation of tumor grade in gliomas. Clin Neurol Neurosurg 107(3):174–180CrossRefPubMed
4.
Zurück zum Zitat Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, Okuda T, Liang L, Ge Y, Komohara Y, Ushio Y (1999) Usefulness of diffusion weighted MRI with echo planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9(1):53–60CrossRefPubMed Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, Okuda T, Liang L, Ge Y, Komohara Y, Ushio Y (1999) Usefulness of diffusion weighted MRI with echo planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9(1):53–60CrossRefPubMed
5.
Zurück zum Zitat Murakami R, Hirai T, Kitajima M, Fukuoka H, Toya R, Nakamura H, Kuratsu J, Yamashita Y (2008) Magnetic resonance imaging of pilocytic astrocytomas: usefulness of the minimum apparent diffusion coefficient (ADC) value for differentiation from high-grade gliomas. Acta Radiol 49(4):462–467CrossRefPubMed Murakami R, Hirai T, Kitajima M, Fukuoka H, Toya R, Nakamura H, Kuratsu J, Yamashita Y (2008) Magnetic resonance imaging of pilocytic astrocytomas: usefulness of the minimum apparent diffusion coefficient (ADC) value for differentiation from high-grade gliomas. Acta Radiol 49(4):462–467CrossRefPubMed
6.
Zurück zum Zitat Tropine A, Vucurevic G, Delani P, Boor S, Hopf N, Bohl J, Stoeter P (2004) Contribution of diffusion tensor imaging to delineation of gliomas and glioblastomas. J Magn Reson Imaging 20(6):905–912CrossRefPubMed Tropine A, Vucurevic G, Delani P, Boor S, Hopf N, Bohl J, Stoeter P (2004) Contribution of diffusion tensor imaging to delineation of gliomas and glioblastomas. J Magn Reson Imaging 20(6):905–912CrossRefPubMed
7.
Zurück zum Zitat Server A, Graff BA, Josefsen R, Orheim TE, Schellhorn T, Nordhøy W, Nakstad PH (2014) Analysis of diffusion tensor imaging metrics for gliomas grading at 3T. Eur J Radiol 83(3):e156–e165CrossRefPubMed Server A, Graff BA, Josefsen R, Orheim TE, Schellhorn T, Nordhøy W, Nakstad PH (2014) Analysis of diffusion tensor imaging metrics for gliomas grading at 3T. Eur J Radiol 83(3):e156–e165CrossRefPubMed
8.
Zurück zum Zitat Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201(3):637–648CrossRefPubMed Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201(3):637–648CrossRefPubMed
9.
Zurück zum Zitat Mamata H, Jolesz FA, Maier SE (2004) Characterization of central nervous system structures by magnetic resonance diffusion anisotropy. Neurochem Int 45(4):553–560CrossRefPubMed Mamata H, Jolesz FA, Maier SE (2004) Characterization of central nervous system structures by magnetic resonance diffusion anisotropy. Neurochem Int 45(4):553–560CrossRefPubMed
10.
Zurück zum Zitat Price SJ, Burnet NG, Donovan T, Green HAL, Pea A, Antoun NM, Pickard JD, Carpenter TA, Gillard JH (2003) Diffusion tensor imaging of brain tumours at 3T: a potential tool for assessing white matter tract invasion? Clin Radiol 58(6):455–462CrossRefPubMed Price SJ, Burnet NG, Donovan T, Green HAL, Pea A, Antoun NM, Pickard JD, Carpenter TA, Gillard JH (2003) Diffusion tensor imaging of brain tumours at 3T: a potential tool for assessing white matter tract invasion? Clin Radiol 58(6):455–462CrossRefPubMed
11.
Zurück zum Zitat Provenzale JM, McGraw P, Mhatre P, Guo AC, Delong D (2004) Peritumoral brain regions in gliomas and meningiomas: investigation with isotropic diffusion-weighted MR imaging and diffusion-tensor MR imaging. Radiology 232(2):451–460CrossRefPubMed Provenzale JM, McGraw P, Mhatre P, Guo AC, Delong D (2004) Peritumoral brain regions in gliomas and meningiomas: investigation with isotropic diffusion-weighted MR imaging and diffusion-tensor MR imaging. Radiology 232(2):451–460CrossRefPubMed
12.
Zurück zum Zitat Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. Journal of Magnetic Resonance, Series B 103(3):247–254CrossRef Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. Journal of Magnetic Resonance, Series B 103(3):247–254CrossRef
13.
Zurück zum Zitat Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36(6):893–906CrossRefPubMed Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36(6):893–906CrossRefPubMed
14.
Zurück zum Zitat Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 17(3):1429–1436CrossRefPubMed Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 17(3):1429–1436CrossRefPubMed
15.
Zurück zum Zitat 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):1432–1440CrossRefPubMed 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):1432–1440CrossRefPubMed
16.
Zurück zum Zitat Hui ES, Cheung MM, Qi L, Wu EX (2008) Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis. NeuroImage 42(1):122–134CrossRefPubMed Hui ES, Cheung MM, Qi L, Wu EX (2008) Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis. NeuroImage 42(1):122–134CrossRefPubMed
17.
Zurück zum Zitat Raab P, Hattingen E, Franz K, Zanella FE, Lanfermann H (2010) Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. Radiology 254(3):876–881CrossRefPubMed Raab P, Hattingen E, Franz K, Zanella FE, Lanfermann H (2010) Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. Radiology 254(3):876–881CrossRefPubMed
18.
Zurück zum Zitat Van Cauter S, Veraart J, Sijbers J, Peeters RR, Himmelreich U, De Keyzer F, Van Gool SW, Van Calenbergh F, De Vleeschouwer S, Van Hecke W, Sunaert S (2012) Gliomas: diffusion kurtosis MR imaging in grading. Radiology 263(2):492–501CrossRefPubMed Van Cauter S, Veraart J, Sijbers J, Peeters RR, Himmelreich U, De Keyzer F, Van Gool SW, Van Calenbergh F, De Vleeschouwer S, Van Hecke W, Sunaert S (2012) Gliomas: diffusion kurtosis MR imaging in grading. Radiology 263(2):492–501CrossRefPubMed
19.
Zurück zum Zitat Davnall F, Yip CS, Ljungqvist G, Selmi M, Ng F, Sanghera B, Ganeshan B, Miles KA, Cook GJ, Goh V (2012) Assessment of tumor heterogeneity: an emerging imaging tool for clinical practice? Insights into imaging 3(6):573–589CrossRefPubMedPubMedCentral Davnall F, Yip CS, Ljungqvist G, Selmi M, Ng F, Sanghera B, Ganeshan B, Miles KA, Cook GJ, Goh V (2012) Assessment of tumor heterogeneity: an emerging imaging tool for clinical practice? Insights into imaging 3(6):573–589CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Marusyk A, Almendro V, Polyak K (2012) Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer 12(5):323–334CrossRefPubMed Marusyk A, Almendro V, Polyak K (2012) Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer 12(5):323–334CrossRefPubMed
21.
Zurück zum Zitat Ryu YJ, Choi SH, Park SJ, Yun TJ, Kim JH, Sohn CH (2014) Glioma: application of whole-tumor texture analysis of diffusion-weighted imaging for the evaluation of tumor heterogeneity. PLoS One 9(9):e108335CrossRefPubMedPubMedCentral Ryu YJ, Choi SH, Park SJ, Yun TJ, Kim JH, Sohn CH (2014) Glioma: application of whole-tumor texture analysis of diffusion-weighted imaging for the evaluation of tumor heterogeneity. PLoS One 9(9):e108335CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Miles KA, Ganeshan B, Griffiths MR, Young RC, Chatwin CR (2009) Colorectal cancer: texture analysis of portal phase hepatic CT images as a potential marker of survival. Radiology 250(2):444–452CrossRefPubMed Miles KA, Ganeshan B, Griffiths MR, Young RC, Chatwin CR (2009) Colorectal cancer: texture analysis of portal phase hepatic CT images as a potential marker of survival. Radiology 250(2):444–452CrossRefPubMed
23.
Zurück zum Zitat Donahue MJ, Blakeley JO, Zhou J, Pomper MG, Laterra J, van Zijl P (2008) Evaluation of human brain tumor heterogeneity using multiple T1 based MRI signal weighting approaches. Magn Reson Med 59(2):336–344CrossRefPubMedPubMedCentral Donahue MJ, Blakeley JO, Zhou J, Pomper MG, Laterra J, van Zijl P (2008) Evaluation of human brain tumor heterogeneity using multiple T1 based MRI signal weighting approaches. Magn Reson Med 59(2):336–344CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Hilario A, Ramos A, Perez-Nuez A, Salvador E, Millan JM, Lagares A, Sepulveda JM, Gonzalez-Leon P, Hernandez-Lain A, Ricoy JR (2012) The added value of apparent diffusion coefficient to cerebral blood volume in the preoperative grading of diffuse gliomas. AJNR Am J Neuroradiol 33:701–707CrossRefPubMed Hilario A, Ramos A, Perez-Nuez A, Salvador E, Millan JM, Lagares A, Sepulveda JM, Gonzalez-Leon P, Hernandez-Lain A, Ricoy JR (2012) The added value of apparent diffusion coefficient to cerebral blood volume in the preoperative grading of diffuse gliomas. AJNR Am J Neuroradiol 33:701–707CrossRefPubMed
25.
Zurück zum Zitat Lee EJ, Lee SK, Agid R, Bae JM, Keller A (2008) Preoperative grading of presumptive low-grade astrocytomas on MR imaging: diagnostic value of minimum apparent diffusion coefficient. Am J Neuroradiol 29(10):1872–1877CrossRefPubMed Lee EJ, Lee SK, Agid R, Bae JM, Keller A (2008) Preoperative grading of presumptive low-grade astrocytomas on MR imaging: diagnostic value of minimum apparent diffusion coefficient. Am J Neuroradiol 29(10):1872–1877CrossRefPubMed
26.
Zurück zum Zitat Mohammadi S, Mller HE, Kugel H, Mller DK, Deppe M (2010) Correcting eddy current and motion effects by affine whole brain registrations: evaluation of three dimensional distortions and comparison with slicewise correction. Magn Reson Med 64(4):1047–1056CrossRefPubMed Mohammadi S, Mller HE, Kugel H, Mller DK, Deppe M (2010) Correcting eddy current and motion effects by affine whole brain registrations: evaluation of three dimensional distortions and comparison with slicewise correction. Magn Reson Med 64(4):1047–1056CrossRefPubMed
27.
Zurück zum Zitat Penny WD, Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE (2011) Statistical parametric mapping: the analysis of functional brain images. Academic press Penny WD, Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE (2011) Statistical parametric mapping: the analysis of functional brain images. Academic press
28.
Zurück zum Zitat Tabesh A, Jensen JH, Ardekani BA, Helpern JA (2011) Estimation of tensors and tensor derived measures in diffusional kurtosis imaging. Magn Reson Med 65(3):823–836CrossRefPubMed Tabesh A, Jensen JH, Ardekani BA, Helpern JA (2011) Estimation of tensors and tensor derived measures in diffusional kurtosis imaging. Magn Reson Med 65(3):823–836CrossRefPubMed
29.
Zurück zum Zitat Skogen K, Ganeshan B, Good T, Critchley G, Miles KA (2011) Imaging heterogeneity in gliomas using texture analysis. Cancer Imaging 11:S113CrossRef Skogen K, Ganeshan B, Good T, Critchley G, Miles KA (2011) Imaging heterogeneity in gliomas using texture analysis. Cancer Imaging 11:S113CrossRef
30.
Zurück zum Zitat Gonzalez, R.C. and Woods, R.E., (2008). Digital image processing. Nueva Jersey. Gonzalez, R.C. and Woods, R.E., (2008). Digital image processing. Nueva Jersey.
31.
Zurück zum Zitat George Stockman and Linda G. Shapiro. (2001). Computer vision (1st ed.). Prentice Hall PTR, Upper Saddle River. George Stockman and Linda G. Shapiro. (2001). Computer vision (1st ed.). Prentice Hall PTR, Upper Saddle River.
32.
Zurück zum Zitat Baldi, I. and Loiseau, H., (2012). Epidemiology of primary brain tumors. In: Tumors of the central nervous system, volume 4 (pp. 3–13). Springer, Netherlands. Baldi, I. and Loiseau, H., (2012). Epidemiology of primary brain tumors. In: Tumors of the central nervous system, volume 4 (pp. 3–13). Springer, Netherlands.
33.
Zurück zum Zitat Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996CrossRefPubMed Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996CrossRefPubMed
34.
Zurück zum Zitat Jolapara M, Patro SN, Kesavadas C, Saini J, Thomas B, Gupta AK, Bodhey N, Radhakrishnan VV (2011) Can diffusion tensor metrics help in preoperative grading of diffusely infiltrating astrocytomas? A retrospective study of 36 cases. Neuroradiology 53(1):63–68CrossRefPubMed Jolapara M, Patro SN, Kesavadas C, Saini J, Thomas B, Gupta AK, Bodhey N, Radhakrishnan VV (2011) Can diffusion tensor metrics help in preoperative grading of diffusely infiltrating astrocytomas? A retrospective study of 36 cases. Neuroradiology 53(1):63–68CrossRefPubMed
35.
Zurück zum Zitat White ML, Zhang Y, Yu F, Kazmi SJ (2011) Diffusion tensor MR imaging of cerebral gliomas: evaluating fractional anisotropy characteristics. Am J Neuroradiol 32(2):374–381CrossRefPubMed White ML, Zhang Y, Yu F, Kazmi SJ (2011) Diffusion tensor MR imaging of cerebral gliomas: evaluating fractional anisotropy characteristics. Am J Neuroradiol 32(2):374–381CrossRefPubMed
36.
Zurück zum Zitat Tozer DJ, JÃger HR, Danchaivijitr N, Benton CE, Tofts PS, Rees JH, Waldman AD (2007) Apparent diffusion coefficient histograms may predict low grade glioma subtype. NMR Biomed 20(1):49–57CrossRefPubMed Tozer DJ, JÃger HR, Danchaivijitr N, Benton CE, Tofts PS, Rees JH, Waldman AD (2007) Apparent diffusion coefficient histograms may predict low grade glioma subtype. NMR Biomed 20(1):49–57CrossRefPubMed
37.
Zurück zum Zitat Kang Y, Choi SH, Kim YJ, Kim KG, Sohn CH, Kim JH, Yun TJ, Chang KH (2011) Gliomas: histogram analysis of apparent diffusion coefficient maps with standard- or high-b-value diffusion-weighted MR imaging—correlation with tumor grade. Radiology 261(3):882–890CrossRefPubMed Kang Y, Choi SH, Kim YJ, Kim KG, Sohn CH, Kim JH, Yun TJ, Chang KH (2011) Gliomas: histogram analysis of apparent diffusion coefficient maps with standard- or high-b-value diffusion-weighted MR imaging—correlation with tumor grade. Radiology 261(3):882–890CrossRefPubMed
38.
Zurück zum Zitat Jiang R, Jiang J, Zhao L, Zhang J, Zhang S, Yao Y, Yang S, Shi J, Shen N, Su C, Zhang J (2015) Diffusion kurtosis imaging can efficiently assess the glioma grade and cellular proliferation. Oncotarget 6(39):42380PubMedPubMedCentral Jiang R, Jiang J, Zhao L, Zhang J, Zhang S, Yao Y, Yang S, Shi J, Shen N, Su C, Zhang J (2015) Diffusion kurtosis imaging can efficiently assess the glioma grade and cellular proliferation. Oncotarget 6(39):42380PubMedPubMedCentral
39.
Zurück zum Zitat Stadlbauer A, Ganslandt O, Buslei R, Hammen T, Gruber S, Moser E, Buchfelder M, Salomonowitz E, Nimsky C (2006) Gliomas: histopathologic evaluation of changes in directionality and magnitude of water diffusion at diffusion-tensor MR imaging. Radiology 240(3):803–810CrossRefPubMed Stadlbauer A, Ganslandt O, Buslei R, Hammen T, Gruber S, Moser E, Buchfelder M, Salomonowitz E, Nimsky C (2006) Gliomas: histopathologic evaluation of changes in directionality and magnitude of water diffusion at diffusion-tensor MR imaging. Radiology 240(3):803–810CrossRefPubMed
Metadaten
Titel
Assessment of tissue heterogeneity using diffusion tensor and diffusion kurtosis imaging for grading gliomas
verfasst von
Rajikha Raja
Neelam Sinha
Jitender Saini
Anita Mahadevan
KVL Narasinga Rao
Aarthi Swaminathan
Publikationsdatum
29.10.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Neuroradiology / Ausgabe 12/2016
Print ISSN: 0028-3940
Elektronische ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-016-1758-y

Weitere Artikel der Ausgabe 12/2016

Neuroradiology 12/2016 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.