Petra Hnilicová1, Soňa Bálentová2, Dagmar Kalenská 3, Eva Hajtmanová 4, Peter Murín 4, Michal Bittšanský1, Marian Adamkov 2, Ján Lehotský3, and Dušan Dobrota 3
1Division of Neurosciences at Biomedical Center Martin, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovakia, 2Institute of Histology and Embryology, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovakia, 3Department of Medical Biochemistry, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovakia, 4Department of Radiotherapy and Oncology, University Hospital Martin, Martin, Slovakia
Synopsis
We investigated the metabolic
effect of a clinically relevant craniospinal irradiation on the rat spinal cord
using 1H MRS at 7T. Hundred days after the fractionated irradiation performed
by radioactive isotope 60Co (16Gy in 2 fractions), irradiated and
sham-irradiated animals underwent in vivo
1H MRS examination. Spinal cord spectra were measured by SVS
sequence with voxel size of 3.5x2x7.5mm3. In spinal cord of
irradiated animals was confirmed significantly reduced tNAA/tCr and increased
tCho/tCr ratio, both showing demyelination and inflammatory processes. It seems
that in vivo 1H MRS of
spinal cord could be useful for radiation therapy monitoring.
PURPOSE
Radiation-induced brain injury usually occurs after
conventional radiation therapy of patients with primary brain tumors and metastases
and is caused by
microstructural and/or metabolic changes in neural tissue.1 It may
have an immediate and strong impact on quality of life, especially when
occurring in the spinal cord.1,2 Although animal models enable to
imitate mechanisms of irradiated injury, it is only poorly explored the late
response of the juvenile rat brain to a clinically relevant fractionated
irradiation.3 Therefore, the aim of this 1H MRS
study was to investigate the metabolic changes in spinal cord induced by the fractionated
craniospinal irradiation with a biological effective dose (BED; 117 Gy)
equivalent to the treatment dose used in many tumor modalities.4METHODS
Three months old Wistar male
rats (n=16) underwent the experiment. Radiation was delivered to
anesthetized rats (n=8) by Teragam KO-2 device (UJP, Prague, Czech
Republic) using the radioactive isotope 60Co with the energy of 1.17 and
1.33MeV. The craniospinal irradiation with BED of 117Gy was delivered in 8Gy
per fraction during 2 consecutive weeks (total dose of 16Gy). The irradiated
and sham-irradiated animals (n=8) survived ~100 days after the irradiation
procedure. In vivo 1H MRS
examinations were performed on 7T small animal MR scanner (Bruker BioSpec 70/20
USR) using a combination of the volume resonator and the 1H receive-only
surface coil with 20mm diameter (Bruker BioSpin MRI, Ettlingen, Germany). Anatomical
images in all orthogonal directions were measured using fast T2-weighted
turbo-spin-echo sequences (turboRARE; TR/TE=2500/33ms; NA=2; echo spacing=10ms;
FOV=35x35mm2; matrix=256x256; 23 slices with a 0.5mm slice
thickness; acquisition time ~2min). Single-voxel 1H MRS data in
the spinal cord (C2-C4) were obtain within ~5min (PRESS; TR/TE=1500/20ms; voxel
size=3.5x2x7.5mm3; NA=200; OVS & VAPOR suppression). Linear and
second order shims were adjusted with the automatic cuboid shim volume with the
water linewidths ~20Hz. Each measured 1H MR spectra (Figure) was analyzed using LCModel and
following metabolites were quantified: N-acetyl-aspartate & N-acetyl-aspartyl-glutamate
(tNAA), choline (phosphatidylcholine, glycerophosphatidylcholine,
acetylcholine, and choline; tCho) and creatine (creatine and
phosphocreatine; tCr) containing
compounds, glutamate
& glutamine (Glx), Gamma-aminobutyric
acid (GABA), and Lactate (Lac). Metabolite ratios to tCr were calculated and
statistically evaluated using the SPSS package (independent-samples
2-tailed t-tests).RESULTS
Quantification of 1H MRS metabolite ratios
in the spinal cord of irradiated animals showed significant decrease of tNAA/tCr
(p=0.003) and significant increase of tCho/tCr (p=0.007),
compare to the animal control group (Table).DISCUSSION
The rat spinal cord after the craniospinal irradiation
with clinically relevant fractionated doses demonstrates some metabolic
abnormalities. Reduced tNAA/tCr manifests damaged neurons caused by neuronal
dysfunction and apoptosis secondary to irradiation.1,5 Considering tCho as a marker of myelin sheath integrity6, the increased
tCho/tNAA found in our study may indicate destruction of myelin sheath or myelin-producing
oligodendrocytes.5,6,7 Since the highest levels of Cr and Cho are
found in oligodendrocytes and astrocytes6, their elevation may also represent
inflammation, de- or re-myelination and ongoing gliosis.1,3,5CONCLUSION
It seems, that clinically relevant fractionated craniospinal
irradiation strongly affects the spinal cord consisting of essential bundles of
motor and sensory tracts. Therefore, the potential clinical application of in vivo 1H MRS
during radiation treatment could be useful for planning of a successful
pharmacological, surgical, or rehabilitative therapy.Acknowledgements
This study was supported by the grant APVV-14-0088 and
by projects: Biomedical Center Martin (ITMS: 26220220187), VEGA 1/0129/16, and VEGA 1/0128/16, co-funded from EU sources.References
-
Greene-Schloesser
D, Robbins
ME, Peiffer
AM, et al. Radiation-induced brain injury: a review. Front Oncol. 2012; 2: 73.
- Hock A, Henning A, Boesiger P, Kollias SS. 1H-MR
Spectroscopy in the Human Spinal Cord. AJNR Am J Neuroradiol. 2013; 20.
- Brown RJ, Jun BJ, Cushman JD,
et al. Changes in imaging and cognition in juvenile rats after whole-brain irradiation.
Int J Radiat
Oncol Biol Phys. 2016;
96(2): 470-8.
- Fowler
JF. 21 years of biologically effective dose, Br J Radiol. 2010; 83(991): 554–568.
- Sundgren PC, Cao Y. Brain irradiation: Effects on
normal brain parenchyma and radiation injury. Neuroimaging
Clin. N. Am. 2009; 19:657-668.
- Soares DP, Law M. Magnetic resonance
spectroscopy of the brain: review of metabolites and clinical applications.
Clinical radiology. 2009; 64(1):12-21.
- Virta
A, Patronas N, Raman R, et al. Spectroscopic imaging of radiation-induced
effects in the white matter of glioma patients. Magn. Reson. Imaging. 2000; 18:
851-857.