Multi-nuclear sodium, diffusion, and perfusion MRI in human gliomas

Nicholas S Cho; Francesco Sanvito; Shruti Thakuria; Chencai Wang; Akifumi Hagiwara; Raksha Nagaraj; Sonoko Oshima; Alfredo L Lopez Kolkovsky; Jianwen Lu; Catalina Raymond; Linda M Liau; Richard G Everson; Kunal S Patel; Won Kim; Isaac Yang; Marvin Bergsneider; Phioanh L Nghiemphu; Albert Lai; David A Nathanson; Timothy F Cloughesy; Benjamin M Ellingson

doi:10.1007/s11060-023-04363-x

Multi-nuclear sodium, diffusion, and perfusion MRI in human gliomas

J Neurooncol. 2023 Jun;163(2):417-427. doi: 10.1007/s11060-023-04363-x. Epub 2023 Jun 9.

Authors

Nicholas S Cho^{1

2

3

4}, Francesco Sanvito^{1

2}, Shruti Thakuria^{1

2}, Chencai Wang^{1

2}, Akifumi Hagiwara^{1

2

5}, Raksha Nagaraj^{1

2}, Sonoko Oshima^{1

2}, Alfredo L Lopez Kolkovsky^{1

2

6}, Jianwen Lu^{1

2}, Catalina Raymond^{1

2}, Linda M Liau⁷, Richard G Everson⁷, Kunal S Patel⁷, Won Kim⁷, Isaac Yang⁷, Marvin Bergsneider⁷, Phioanh L Nghiemphu^{8

9}, Albert Lai^{8

9}, David A Nathanson¹⁰, Timothy F Cloughesy^{8

9}, Benjamin M Ellingson^{11

12

13

14

15

16}

Affiliations

¹ UCLA Brain Tumor Imaging Laboratory (BTIL), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, CA, USA.
² Department of Radiological Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
³ Department of Bioengineering, Henry Samueli School of Engineering and Applied Science, University of California, Los Angeles, Los Angeles, CA, USA.
⁴ Medical Scientist Training Program, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
⁵ Department of Radiology, Juntendo University School of Medicine, Tokyo, Japan.
⁶ NMR Laboratory, Neuromuscular Investigation Center, Institute of Myology, Paris, France.
⁷ Department of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
⁸ UCLA Neuro-Oncology Program, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
⁹ Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
¹⁰ Department of Molecular and Medical Pharmacology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
¹¹ UCLA Brain Tumor Imaging Laboratory (BTIL), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, CA, USA. bellingson@mednet.ucla.edu.
¹² Department of Radiological Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA. bellingson@mednet.ucla.edu.
¹³ Department of Bioengineering, Henry Samueli School of Engineering and Applied Science, University of California, Los Angeles, Los Angeles, CA, USA. bellingson@mednet.ucla.edu.
¹⁴ Department of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA. bellingson@mednet.ucla.edu.
¹⁵ Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA. bellingson@mednet.ucla.edu.
¹⁶ UCLA Brain Tumor Imaging Laboratory (BTIL) Professor of Radiology, Psychiatry, and Neurosurgery Departments of Radiological Sciences, Psychiatry, and Neurosurgery David Geffen School of Medicine, University of California, Los Angeles, 924 Westwood Blvd., Suite 615, Los Angeles, CA, 90024, USA. bellingson@mednet.ucla.edu.

Abstract

Purpose: There is limited knowledge about the associations between sodium and proton MRI measurements in brain tumors. The purpose of this study was to quantify intra- and intertumoral correlations between sodium, diffusion, and perfusion MRI in human gliomas.

Methods: Twenty glioma patients were prospectively studied on a 3T MRI system with multinuclear capabilities. Three mutually exclusive tumor volumes of interest (VOIs) were segmented: contrast-enhancing tumor (CET), T2/FLAIR hyperintense non-enhancing tumor (NET), and necrosis. Median and voxel-wise associations between apparent diffusion coefficient (ADC), normalized relative cerebral blood volume (nrCBV), and normalized sodium measurements were quantified for each VOI.

Results: Both relative sodium concentration and ADC were significantly higher in areas of necrosis compared to NET (P = 0.003 and P = 0.008, respectively) and CET (P = 0.02 and P = 0.02). Sodium concentration was higher in CET compared to NET (P = 0.04). Sodium and ADC were higher in treated compared to treatment-naïve gliomas within NET (P = 0.006 and P = 0.01, respectively), and ADC was elevated in CET (P = 0.03). Median ADC and sodium concentration were positively correlated across patients in NET (r = 0.77, P < 0.0001) and CET (r = 0.84, P < 0.0001), but not in areas of necrosis (r = 0.45, P = 0.12). Median nrCBV and sodium concentration were negatively correlated across patients in areas of NET (r=-0.63, P = 0.003). Similar associations were observed when examining voxel-wise correlations within VOIs.

Conclusion: Sodium MRI is positively correlated with proton diffusion MRI measurements in gliomas, likely reflecting extracellular water. Unique areas of multinuclear MRI contrast may be useful in future studies to understand the chemistry of the tumor microenvironment.

Keywords: Diffusion MRI; Dynamic susceptibility contrast perfusion MRI; Glioblastoma; Glioma; Multinuclear MRI; Sodium MRI.

MeSH terms

Brain Neoplasms* / diagnostic imaging
Brain Neoplasms* / pathology
Diffusion Magnetic Resonance Imaging
Glioma* / diagnostic imaging
Glioma* / pathology
Humans
Magnetic Resonance Imaging
Necrosis
Perfusion
Protons
Tumor Microenvironment

Substances

Protons

Abstract

MeSH terms

Substances

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