Original Article

Comparison of Ultrasonographic Images of Glioblastoma Tumor with Magnetic Resonance Images: Rat Animal Model

Abstract

Purpose: Magnetic Resonance Imaging (MRI) can guide the surgical strategy to identify brain tumors and monitor treatment response. It is possible to use transcranial Ultrasound (US) for periodical follow-ups. Ultrasound waves pass through the delicate areas of the skull called acoustic windows. In this study, the efficiency of ultrasound imaging was performed to diagnose glioblastoma brain tumors and the results were compared with MR images.
Materials and Methods: Male Wistar rats were anesthetized by intraperitoneal injection of Ketamine and Xylazine. A stereotaxic device was used to determine the injection coordinates. C6 GBM cell lines were injected into the brains of rats. After two weeks, the formation of a glioblastoma tumor was confirmed histopathologically. The brain of animals was imaged by B-mode ultrasound and MRI. The section with the largest tumor dimensions was selected and the dimensions of the skull and tumor were measured based on the pixel size of each of the imaging methods. Pearson coefficient of correlation and Limits Of Agreement (LOA) were calculated for comparisons of the skull and tumor dimensions.
Results: The skull and the tumor dimensions showed a significant correlation between the B-mode ultrasound and the MRI measurements (R=0.99 and p<0.05). According to the Bland-Altman analysis, the mean difference was 0.31 mm (SD=0.20) for skull and tumor dimensions. The exact shape of the tumor is not completely clear in the ultrasound images, but it can be useful to detect the presence of the tumor and its approximate dimensions.
Conclusion: In conclusion, a glioblastoma tumor was produced in the male Wistar rat. The tumor dimensions were properly assessed by B-mode ultrasound image processing and compared with MR imaging.

1- Thust, S.C. et al., "Glioma imaging in Europe: a survey of 2centersres and recommendations for best clinical practice." European radiology, Vol. 28 (No. 8), pp. 3306-3317 (2018).
2- Hemphill, J.C. et al., "Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American heart Association/American stroke association." Stroke, Vol. 46 (No. 7), pp. 2032–2060 (2015).
3- Dastur, C.K. et al., "Current management of spontaneous intracerebral hemorrhage." Stroke and Vascular Neurology, Vol. 2 (No. 1), pp. 21–29 (2017).
4- Lin, J.B. et al., "Imaging of small animal peripheral artery disease models: recent advancements and translational potential." International Journal of Molecular Sciences, Vol. 16 (No. 5), pp. 11131–11177 (2015).
5- Meyer-Wiethe, K. et al., "Diagnosis of intracerebral hemorrhage with transcranial ultrasound." Cerebrovascular Diseases, Vol. 27 (No. 2), pp. 40–47 (2009).
6- Blanco, P. et al., "Intracranial hematoma and midline shift detected by transcranial color-coded duplex sonography." The American Journal of Emergency Medicine, Vol. 33 (No. 11), pp. 1715.e5-1715.e7 (2015).
7- Greco, A. et al., "Ultrasound biomicroscopy in small animal research: applications in molecular and preclinical imaging. " Journal of Biomedicine and Biotechnology, Vol. 2012, pp. 1-14, (2012).
8- Maresca, D. et al., "Biomolecular ultrasound and sonogenetics. " Annual Review of Chemical and Biomolecular Engineering, Vol. 9, pp. 229–252 (2018).
9- Fry, F.J. et al., "Acoustical properties of the human skull. " Journal of the Acoustical Society of America, Vol. 63, pp. 1576–1590 (1978).
10- Kirkham, F.J. et al., "Transcranial measurement of blood velocities in the basal cerebral arteries using pulsed Doppler ultrasound: velocity as an index of flow. " Ultrasound in Medicine and Biology, Vol. 12, pp. 15–21 (1986).
11- Smith, S.W. et al., "Feasibility study: Real-time 3-D ultrasound imaging of the brain. " Ultrasound in Medicine and Biology, Vol. 30, pp. 1365–1371 (2004).
12- Lindsey, B.D. et al., "Simultaneous bilateral real-time 3-D transcranial ultrasound imaging at 1 MHz through poor acoustic windows. " Ultrasound in Medicine and Biology, Vol. 39, pp. 721–734 (2013).
13- Graham Michelle T. et al., "Investigation of acoustic windows for photoacoustic imaging of intracranial blood vessels." In 2020 IEEE International Ultrasonics Symposium (IUS), pp. 1-4 (2020).
14- Li, H. et al., "The Thickness Measurement of Alive Human Skull Based on CT Image. " Journal of Biomedical Engineering, Vol. 24, pp. 964–968 (2007).
15- Okita, K. et al., "The role of numerical simulation for the development of an advanced HIFU system. " Computational Applied Mechanics, Vol. 54, pp. 1023-1033 (2014).
16- Samoudi, M. et al., "Computational modeling of a single-element transcranial focused ultrasound transducer for subthalamic nucleus stimulation. " Neural Engineering, Vol. 16, pp. 026015 (2019).
17- Gatto, M. et al., "Three-Dimensional Printing (3DP) of neonatal head phantom for ultrasound: Thermocouple embedding and simulation of bone. " Medical Engineering and Physics, Vol. 34, pp. 929–937 (2012).
18- Saito, O. et al., "Substantial fluctuation of acoustic intensity transmittance through a bone-phantom plate and its equalization by modulation of ultrasound frequency. " Ultrasonics, Vol. 59, pp. 94-101 (2015).
19- Pichardo, S. et al., "Multi-frequency characterization of the speed of sound and attenuation coefficient for longitudinal transmission of freshly excised human skulls. " Physics in Medicine and Biology, Vol. 56, pp. 219 (2011).
20- Boutet, A. et al., "The relevance of skull density ratio in selecting candidates for transcranial MR-guided focused ultrasound. " Journal of Neurosurgery, Vol. 132, pp. 1785–1791 (2020).
21- Giustetto, P. et al., "Non-invasive parenchymal, vascular and metabolic high-frequency ultrasound and photoacoustic rat deep brain imaging." Journal of Visualized Experiments, Vol. 2015 (No. 97), pp. 4–5 (2015).
22- Mac´E, E. et al., "Functional ultrasound imaging of the brain." Nature Methods, Vol. 8 (No. 8), pp. 662–664 (2011).
23- Osmanski, B.F. et al., "Functional ultrasound imaging of intrinsic connectivity in the living rat brain with high spatiotemporal resolution." Nature Communications, Vol. 5 (No. 5023), pp. 1-14 (2014).
24- Brunner, C. et al., "Mapping the dynamics of brain perfusion using functional ultrasound in a rat model of transient middle cerebral artery occlusion." Journal of Cerebral Blood Flow and Metabolism, Vol. 37 (No. 1), pp. 263-276 (2017).
25- Mac´e, E. et al., "In vivo mapping of brain elasticity in small animals using shear wave imaging." IEEE Transactions on Medical Imaging, Vol. 30 (No. 3), pp. 550–558 (2011).
26- Dill, T., "Contraindications to magnetic resonance imaging: non-invasive imaging. " Heart, Vol. 94 (No. 7), pp. 943–948 (2008).
27- Meyer, K. et al., "Transcranial sonography of brain tumors in the adult: an in vitro and in vivo study. " Journal of Neuroimaging, Vol. 11 (No. 3), pp. 287-292 (2001).
28- Alphandéry, Edouard. "Nano-therapies for glioblastoma treatment." Cancers, Vol. 12 (No. 1), pp. 242 (2020).
29- Gomezmez-de Frutos, M.C. et al., "Identification of brain structures and blood vessels by conventional ultrasound in rats." Journal of Neuroscience Methods, Vol. 346, pp. 108935 (2020).
30- Kilkenny, C. et al., "Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research." PLOS Biology, Vol. 8, pp. 1000412 (2010).
31- Heydarheydari, S. et al., "Pulsed high magnetic field-induced reversible blood-brain barrier
permeability to enhance brain-targeted drug delivery." Electromagnetic Biology and Medicine, Vol. 40 (No. 2), pp. 1-14 (2021).
32- Miura, F.K. et al., "Experimental nodel of C6 brain tumors in athymic rats. " Arquivos de Neuro-Psiquiatria, Vol. 66 (No. 2), pp. 238-241 (2008).
33- Moladoust, H. et al., "Estimation of septal wall thickness by processing sequential echocardiographic images." Iranian Cardiovascular Research Journal Vol. 3, 24-33 (2009).
34- Morelli, L. et al., "Role of abdominal ultrasound for the surveillance follow-up of pancreatic cystic neoplasms: a cost-effective safe alternative to the routine use of magnetic resonance imaging." World Journal of Gastroenterology, Vol. 25 (No. 18), pp. 2217–2228 (2019).
35- Mehrad, H. et al. "Ultrasonographic analysis versus histopathologic evaluation of carotid advanced atherosclerotic stenosis in an experimental rabbit model." Ultrasound in Medicine and Biology, Vol. 38, pp. 1391-1403 (2012).
36- Swanson, D.C. et al., "Validity of ultrasound imaging for intrinsic foot muscle cross-sectional area measurements demonstrated by strong agreement with MRI." BMC Musculoskeletal Disorders, Vol. 23 (No. 1), pp. 1-12 (2022).
37- Yip, A. et al., "Magnetic resonance imaging compared to ultrasonography in giant cell arteritis: a cross-sectional study." Arthritis research and therapy, Vol. 22 (No. 1). pp. 1-8 (2020).
38- Akbari, P. et al., "Total Kidney Volume Measurements in ADPKD by 3D and Ellipsoid Ultrasound in Comparison with Magnetic Resonance Imaging." Clinical Journal of the American Society of Nephrology, Vol. 17 (No. 6), pp. 827-834 (2022).
39- Moura Silva, G.A.P. et al., "Transcranial ultrasonography as a reliable instrument for the measurement of the cerebral ventricles in rats with experimental hydrocephalus: a pilot study. " Child's Nervous System, Vol. 37, pp. 1863–1869 (2021).
40- Gomez -de Frutos M.C. et al., "B-Mode Ultrasound, a Reliable Tool for Monitoring Experimental Intracerebral Hemorrhage. " Frontiers in Neurology, Vol. 12, 771402 (2021).
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IssueVol 11 No 2 (2024) QRcode
SectionOriginal Article(s)
DOI https://doi.org/10.18502/fbt.v11i2.15332
Keywords
Ultrasonography Magnetic Resonance Imaging T2 Weighted Glioblastoma Multiform Tumor

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How to Cite
1.
Shahidani A, Mokhtari Dizaji M, Shankayi Z, Najafi M. Comparison of Ultrasonographic Images of Glioblastoma Tumor with Magnetic Resonance Images: Rat Animal Model. Frontiers Biomed Technol. 2023;11(2):169-176.