Comparison of T2 and T2*-weighted MR molecular imaging of a mouse model of glioma

BMC Medical Imaging

Boguslaw Tomanek⁵  Andre Obenaus⁶  Garnette R Sutherland³  Abedelnasser Abulrob¹  Umar Iqbal¹  Randy Tyson⁴  Wladyslaw P Weglarz²  Dragana Ponjevic⁷  John Matyas⁷  David Rushforth³  Tadeusz Foniok³  Samuel Barnes⁶  Barbara Blasiak² 

[1] Human Health Therapeutics Portfolio, National Research Council of Canada, Ottawa K1A 0R6, Ontario Canada;Polish Academy of Sciences, Institute of Nuclear Physics, Krakow,152 Radzikowskiego, Krakow, Malopolska 31-342, Poland;Department of Clinical Neurosciences and Radiology, University of Calgary, 3330 Hospital Dr NW, Calgary, Alberta T2N 4N1, Canada;Alberta Innovates – Technology Futures, 3608 33 Street NW, Calgary T2L 2A6, Alberta, Canada;Thunder Bay Regional Research Institute, 980 Oliver Road, Thunder Bay, Ontario P7B 6V4, Canada;Departments of Radiation Medicine, Radiology, Pediatrics, Loma Linda University Chan Shun Pavilion, Room A101011175 Campus Street, Loma Linda, California 92354, USA;Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Dr NW, Calgary, Alberta T2N 4N1, Canada

关键词: Glioma;    Contrast agents;    Molecular MRI;    MRI;    Contrast-to-noise ratio;   

Others  :  1090923
DOI  :  10.1186/1471-2342-13-20

 received in 2013-02-18, accepted in 2013-07-17,  发布年份 2013

【 摘 要 】

Background

Standard MRI has been used for high-grade gliomas detection, albeit with limited success as it does not provide sufficient specificity and sensitivity to detect complex tumor structure. Therefore targeted contrast agents based on iron oxide, that shorten mostly T2 relaxation time, have been recently applied. However pulse sequences for molecular imaging in animal models of gliomas have not been yet fully studied. The aim of this study was therefore to compare contrast-to-noise ratio (CNR) and explain its origin using spin-echo (SE), gradient echo (GE), GE with flow compensation (GEFC) as well as susceptibility weighted imaging (SWI) in T2 and T2* contrast-enhanced molecular MRI of glioma.

Methods

A mouse model was used. U87MGdEGFRvIII cells (U87MG), derived from a human tumor, were injected intracerebrally. A 9.4 T MRI system was used and MR imaging was performed on the 10 day after the inoculation of the tumor. The CNR was measured prior, 20 min, 2 hrs and 24 hrs post intravenous tail administration of glioma targeted paramagnetic nanoparticles (NPs) using SE, SWI, GE and GEFC pulse sequences.

Results

The results showed significant differences in CNR among all pulse sequences prior injection. GEFC provided higher CNR post contrast agent injection when compared to GE and SE. Post injection CNR was the highest with SWI and significantly different from any other pulse sequence.

Conclusions

Molecular MR imaging using targeted contrast agents can enhance the detection of glioma cells at 9.4 T if the optimal pulse sequence is used. Hence, the use of flow compensated pulse sequences, beside SWI, should to be considered in the molecular imaging studies.

【 授权许可】

   
2013 Blasiak et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 4.

【 参考文献 】

• [1]Blasiak B, Tomanek B, Abulrob A, Iqbal U, Stanimirovic D, Albaghdadi H, Foniok T, Lun X, Forsyth P, Sutherland RG: Detection of T2 changes in an early mouse brain tumor. Magn Res Imag 2010, 28:784-789.
• [2]Ohagaki H, Kleihues P: Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 2005, 64:479-489.
• [3]Ellegala DB, Leong-Poi H, Carpenter JE, Klibanov AL, Kaul S, Shaffrey ME, Sklenar J, Lindner JR: Imaging tumor angiogenesis with contrast ultrasound and microbubbles targeted to αvß3. Circulation 2003, 108:336-341.
• [4]Aghi M, Gaviani P, Henson JW, Batchelor TT, David N, Louis DN, Barker FG II: Magnetic resonance imaging characteristics predicts epidermal growth factor receptor amplification status in glioblastomas. Clin Cancer Res 2005, 11:8600-8605.
• [5]Veish O, Gunn JW, Zhang M: Design and fabrication of magnetic nanoparticles for targeted drug delivery and therapy. Adv Drug Deliv Rev 2010, 62:284-304.
• [6]Figuerola A, Di Corato R, Manna L, Pelligrino T: From iron oxide nanoparticle towards advanced iron-based inorganic materials designed for biomedical applications. Pharmacol Res 2010, 26:126-143.
• [7]Tomanek B, Iqbal U, Blasiak B, Abulrob A, Albaghdadi H, Matyas JR, Ponjevic D, Sutherland GR: Evaluation of brain tumor vessels specific contrast agents for glioblastoma imaging. Neuro Oncol 2012, 14(1):53-63.
• [8]Das GK, Johnson NJJ, Cramen J, Blasiak B, Latta P, Tomanek B, van Veggel FCJM: NaDyF4 nanoparticle as T2 contrast agent for ultra-high field magnetic resonance imaging. J Phys Chem Lett 2012, 3:524-529.
• [9]Dong C, Korinek A, Blasiak B, Tomanek B, van Veggel F: Cation exchange: a facile method to make NaYF4:Yb, Tm-NaGdF4 core-shell nanoparticles with a thin, tunable, and uniform shell. Chem Mater 2012, 24(7):1297-1305.
• [10]LaConte LE, Nitin N, Zurkiya O, Caruntu D, O’Connor CJ, Hu X, Bao G: Coating thickness of magnetic iron oxide nanoparticles affects R2 relaxivity. J Magn Reson Imag 2007, 26:1634-1641.
• [11]Wang YX, Hussain SM, Krestin GP: Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur Radiol 2001, 11:2319-2331.
• [12]Gambarota G, van Laarhoven HW, Phillipens M, Lok J, van der Kogel A, Punt CJA, Heerschap A: Assessment of absolute blood volume in carcinoma by USPIO contrast-enhanced MRI. Magn Reson Imag 2006, 24:279-286.
• [13]Runge VM, Clanton JA, Partian CL, James AE Jr: Respiratory gating in magnetic resonance imaging at 0.5 Tesla. Radiology 1984, 151:521-523.
• [14]Haacke EM, Patrick JL: Reducing motion artifacts in two-dimensional Fourier transform imaging. Mag Reson Imaging 1986, 4:359-376.
• [15]Bailes DR, Gilderdale DJ, Bydder GM, Collins AG, Firmin DN: Respiratory ordered phase encoding (ROPE): a method for reducing motion artefacts in MR imaging. J Comput Assist Tomogr 1985, 9:835-838.
• [16]Ehman RL, Felmlee FP: Flow artifact reduction in MRI: a review of the roles of gradients moment nulling and spatial presaturation. Magn Reson Med 1990, 14:293-307.
• [17]Haacke EM, Lenz GW: Improving MR image quality in the presence of motion by using rephrasing gradients. AJR Am J Roentgenol 1987, 148:1251-1258.
• [18]Pattaney PM, Philips JJ, Chiu LC, Lipcamon JD, Duerk JL, McNally JM, Mohapatra SN: Motion artifacts suppression technique (MAST) for MR imaging. J Comput Assist Tomogr 1987, 11:369-377.
• [19]Haacke EM, Mittal S, Wue Z, Neelavalli J, Cheng Y-CN: Susceptibility-weighted imaging: technical aspects and clinical applications, part 1. AJNR 2009, 30:19-30.
• [20]Reichenbach JR, Venkatesan R, Schillinger DJ, Kido DK, Haacke EM: Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology 1997, 204:272-277.
• [21]Nishikawa MM, Sant’Anna OD, Lazera MS, Wanke B: Use of D-proline assimilation and CGB medium for screening Brazilian Cryptococcus neoformans. J Med Vet Mycol 1996, 34:365-366.
• [22]Corot C, Robert P, Idee J-M, Port M: Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 2006, 58:1471-1504.
• [23]Gupta AK, Gupta M: Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005, 26(18):3995-4021.
• [24]Amstad E, Zurcher S, Mashaghi A, Wong JY, Textor M, Reimhult E: Surface functionalization of single superparamagnetic iron oxide nanoparticles for targeted magnetic resonance imaging. Small 2009, 5:1334-1342.
• [25]Abulrob N, Veres T, Iqbal U, Stanimirovic D, Tomanek B: Single-domain antibody targeted formulations with superparamagnetic nanoparticles for cancer imaging. US: Provisional Patent; 2009. 61/118,205
• [26]Moller-Hartmann W, Herninghaus S, Krings T, Marquardt G, Lanfermann H, Pilatus U, Zanella FE: Clinical application of proton magnetic resonance spectroscopy in the diagnosis of intracranial mass lesions. Neuroradiology 2002, 44:371-381.
• [27]Lee N, Kim H, Choi SH, Park M, Kim D, Kim HC, Choi Y, Lin S, Kim BH, Jung HS, Kim H, Park KS, Moon WK, Hyeona T: Magnetosome-like ferrimagnetic iron oxide nanocubes for highly sensitive MRI of single cells and transplanted pancreatic islets. Proc Natl Acad Sci USA 2011, 108(7):2662-2667.
• [28]Provias J, Claffey K, DelAguila L, Nelson L, Matthias F, Abhijit G: Meningiomas: role of vascular endothelial growth factor/vascular permeability factor in angiogenesis and peritumoral edema. Neurosurgery 1997, 40:1016-1026.
• [29]Etzioni R, Urban N, Ramsey S, McIntosh M, Schwartz S, Reid B, Radich J, Anderson G, Hartwell L: The case for early detection. Nat Rev Cancer 2003, 3:243-252.
• [30]Stevenson CB, Ehtesham M, McMillan MK, Valadez JG, Edgeworth ML, Price RR, Abel TW, Mapara KY, Thompson RC: CXCR4 expression is elevated in glioblastoma multiforme and correlates with an increase in intensity and extent of peritumoral T2-weighted magnetic resonance imaging signal abnormalities. Neurosurgery 2008, 63:560-569.
• [31]Ehtesham M, Winston JA, Kabos P, Thompson RC: CXCR4 expression mediates glioma cell invasiveness. Oncogene 2006, 25:2801-2806.
• [32]Skong J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Curry WT, Carter BS Jr, Krichevsky AM, Breakefield XO: Gliobliastoma microvesicles transport RNA and proteins that promote tumor growth and provide diagnostic biomarkers. Nat Cell Biol 2008, 10:1470-1476.
• [33]Hammoud MA, Sawaya R, Shi W, et al.: Prognostic significance of preoperative MRI scan in gliobliastoma multiforme. J Neurooncol 1996, 27:65-73.
• [34]Claes A, Idema AJ, Wesseling P: Diffuse glioma growth: a guerilla war. Acta Neuropathol 2007, 114:443-458.
• [35]Tozer GM, Ameer-Beg SM, Baker J, Barber PR, Hill SA, Hodgkiss RJ, Locke R, Prise VE, Wilson I, Vojnovic B: Intravital imaging of tumor vascular networks using multi-photon fluorescence microscopy. Adv Drug Deliver Rev 2005, 57:135-152.
• [36]Kuroiwa T, Cahn R, Juhler M, Goping G, Campbell G, Klatzo I: Role of extracellular proteins in the dynamics of vasogenic brain edema. Acta Neuropathol 1985, 66:3-11.
• [37]Reulen HJ, Graham R, Spatz M, Klatzo I: Role of pressure gradients and bulk flow in dynamics of vasogenic brain edema. J Neurosurgery 1977, 46:24-35.
• [38]Strugar J, Rothbart D, Harrington W, Criscuolo GR: Vascular permeability factor in brain metastases correlation with vasogenic brain edema and tumor angiogenesis. J Neurosurgery 1994, 81:560-566.
• [39]Martin-Villalba A, Okuducu AF, von Deimling A: The evolution of our understanding on glioma. Brain Pathol 2008, 18:455-463.
• [40]Gambarota G, Leenders W, Maass C, Wesseling P, van der Kogel B, van Tellingen O, Heerschap A: Characterisation of tumor vasculature in mouse brain by USPIO contrast-enhanced MRI. Br J Cancer 2008, 98:1784-1789.
• [41]Dennie J, Mandeville JB, Boxerman JL, Packard SD, Rosen BR, Weisskoff RM: NMR imaging of changes in vascular morphology due to tumor angiogenesis. Magn Reson Med 1998, 40:793-799.
• [42]Kennan RP, Zhong J, Gore JC: Intravascular susceptibility contrast mechanisms in tissues. Magn Reson Med 1994, 31:9-21.
• [43]Oostendorp M, Post MJ, Backes WH: Vessel growth and function: depiction with contrast-enhanced MR imaging. Radiology 2009, 251:317-335.
• [44]Lin W, Mukherjee P, An H, Yu Y, Wang Y, Vo K, Lee B, Kido D, Haacke EM: Improving high-resolution MR bold venographic imaging using a T1 reducing contrast agent. J Magn Reson Imag 1999, 10:118-123.
• [45]Urchuk SN, Plewes DB: Mechanisms of flow-induced signal loss in MR angiography. J Magn Reson Imag 1992, 2:453-462.
• [46]Weisskoff RM, Kihne S: MRI susceptometry: image-based measurement of absolute susceptibility of MR contrast agents and human blood. Magn Reson Med 1992, 24:375-383.
• [47]Sedlacik J, Rauscher A, Reichenbach JR: Obtaining blood oxygenation levels from MR Signal behavior in the presence of single venous vessels. Magn Reson Med 2007, 58:1035-1044.
• [48]Denk C, Torres EH, MacKay A, Rauscher A: The influence of white matter fibre orientation on MR signal phase and decay. NMR Biomed 2011, 24:246-252.
• [49]Deistung A, Rauscher A, Sedlacik J, Stadler J, Witoszynskyj S, Reichenbach JR: Susceptibility weighted imaging at ultra high magnetic field strengths: theoretical considerations and experimental results. Magn Reson Med 2008, 60:1155-1168.