Emine Ülkü SARITAŞ, Kalaivani THANGAVEL

Aqueous paramagnetic solutions for MRI phantoms at 3 T: A detailed study on relaxivities

Phantoms with known T1 and T2 values that are prepared using solutions of easily accessible paramagnetic agents are commonly used in MRI imaging centers, especially with the goal of validating the accuracy of quantitative imaging protocols. The relaxivity parameters of several agents were comprehensively examined at lower B 0 field strengths, but studies at 3 T remain limited. The main goal of this study is to measure r 1 and r 2 relaxivities of three common paramagnetic agents (CuSO4 , MnCl 2 , and NiCl 2) at room temperature at 3 T. Separate phantoms were prepared at various concentrations of 0.05 0.5 mM for MnCl 2 and 1 6 mM for CuSO4 and NiCl 2 . For assessment of T1 relaxation times, inversion recovery turbo spin echo images were acquired at 15 inversion times ranging between 24 and 2500 ms. For assessment of T2 relaxation times, spin-echo images were acquired at 15 echo times ranging between 8.5 and 255 ms. Voxel-wise T1 and T2 relaxation times at each concentration were separately determined from the respective signal recovery curves (inversion recovery for T1 and spin echo decay for T2). Relaxivities r 1 and r 2 for all three agents that were derived from these relaxation time measurements are reported: r 1 = 0.602 mM −1 s−1 and r 2 =0.730 mM −1s −1 for CuSO4 , r 1 = 6.397 mM −1 s −1 and r 2 = 108.266 mM −1 s−1 for MnCl 2 , r 1 = 0.620 mM −1 s −1 and r 2 = 0.848 mM −1 s-1 for NiCl 2 . These results will serve as a practical reference to design phantoms of target T1 and T2 values at 3 T, in particular phantoms with relaxation times equivalent to specific human tissues.

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[1] Cheng HL, Stikov N, Ghugre NR, Wright GA. Practical medical applications of quantitative MR relaxometry. J Magn Reson Imaging 2012; 36: 805-824.
[2] Lartigue L, Oumzil K, Guari Y, Lartigue J, Gu´erin C, Montero JL, Barragan MV, Sangregorio C, Caneschi A, Innocenti C et al. Water soluble Rhamnose coated Fe 3 O4 nanoparticles. Org Lett 2009; 11: 2992-2995.
[3] Lartigue L, Innocenti C, Kalaivani T, Awwad A, Sanchez DM, Guari Y, Larionova J, Gu´erin C, Montero JLG, Barragan MV et al. Water-dispersible sugar coated magnetite nanoparticles. An evaluation of their relaxometric and magnetic hyperthermia properties. J Am Chem Soc 2011; 133: 10459-10472.
[4] Carniato F, Thangavel K, Tei L, Botta M. Structure and Dynamics of the Hydration shells of Citrate- coated GdF3 Nanoparticles. J Mater Chem B 2013; 1: 2442-2446.
[5] Bordonali L, Kalaivani T, Sabareesh KPV, Innocenti C, Fantechi E, Sangregorio C, Casula MF, Lartigue L, Larionova J, Guari Y, et.al. NMR-D Study of the Local Spin dynamics and magnetic Anisotropy in different nearly monodispersed Ferrite nanoparticles. J Phys-Condens Mat 2013; 25: 066008(1)-066008(9).
[6] Price RR, Axel L, Morgan T, Newman R, Perman W, Schneiders N, Selikson M, Wood M, Thomas SR. Quality assurance methods and phantoms for magnetic resonance imaging: Report of AAPM nuclear magnetic resonance Task Group No.1. Med Phys 1990; 17: 287-295.
[7] Bucciolini M, Ciraolo L, Renzi R. Relaxation rates of paramagnetic solutions: evaluation by nuclear magnetic resonance imaging. Med Phys 1986; 13: 298-303.
[8] Schneiders NJ. Solutions of two paramagnetic ions for use in nuclear magnetic resonance phantoms. Med Phys 1988; 15: 12-16.
[9] Beall PT, Amtey SR, Kasturi SR. NMR Data Handbook for Biomedical Applications. New York, NY, USA: Pergamon Press, 1984.
[10] Pykett IL, Rosen BR, Buonanno FS, Brady TJ. Measurement of spin-lattice relaxation times in nuclear magnetic resonance imaging. Phys Med Biol 1983; 28: 723-729.
[11] Eunji I, Hani EN, Masoom H. Fabrication and characterization of polymer gel for MRI phantom with embedded lesion particles. P Soc Photo-Opt Ins 2012; 8348: 83480V(1)-83480V(12).
[12] Kato H, Kuroda M, Yoshimura K, Yoshida A, Hanamoto K, Kawasaki S, Shibuya K, Kanazawa S. Composition of MRI phantom equivalent to human tissues. Med Phys 2005; 32: 3199-3208.
[13] Korb JP, Bryant RG. Magnetic field dependence of proton spin-lattice relaxation times. Magn Reson Med 2002; 48: 21-26.
[14] Sasaki M, Shibata E, Kanbara Y, Ehara S. Enhancement effects and relaxivities of gadolinium-DTPA at 1.5 versus 3 Tesla: a phantom study. Magn Reson Med Sci 2005; 4: 145-149.
[15] Jerrolds J, Keene S. MRI safety at 3 T versus 1.5 T. Internet J World Health Soc Politics 2008; 6: 1.
[16] Lawrence NT. 3 T MRI in clinical practice. Appl Radiol 2005; 34: 8-17.
[17] Trattnig S, Ba-Ssalamah A, Noebauer-Huhmann IM, Barth M, Wolfsberger S, Pinker K, Knosp E. MR Contrast agent at high-field MRI (3 Tesla). Top Magn Reson Imag 2003; 14: 365-375.
[18] Hattori K, Ikemoto Y, Takao W, Ohno S, Harimoto T, Kanazawa S, Oita M, Shibuya K, Kuroda M, Kato H. Development of MRI phantom equivalent to human tissues for 3.0-T MRI. Med Phys 2013; 40: 032303(1)- 032303(11).
[19] Simon GH, Bauer J, Saborovski O, Fu Y, Corot C, Wendland MF, Daldrup-Link HE. T1 and T2 relaxivity of intracellular and extracellular USPIO at 1.5 T and 3 T clinical MR scanning. Eur Radiol 2006; 16: 738-745.
[20] Shen Y, Goerner FL, Snyder C, Morelli JN, Hao D, Hu D, Li X, Runge VM. T1 relaxivities of gadolinium-based magnetic resonance contrast agents in human whole blood at 1.5, 3, and 7 T. Invest Radiol 2015; 50: 330-338.
[21] Rohrer M, Bauer H, Mintorovitch J, Requardt M, Weinmann HJ. Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol 2005; 40: 715-724.
[22] Kalavagunta C, Metzger GJ. A field comparison of r1 and r2* relaxivities of Gd-DTPA in aqueous solution and whole blood: 3 T versus 7 T. Proc Int Soc Mag Reson Med 2010; 18: 4990.
[23] Pan D, Caruthers SD, Senpan A, Schmieder AH, Wickline SA, Lanza GM. Revisiting an old friend: manganesebased MRI contrast agents. WIREs Nanomed Nanobiotechnol 2011; 3: 162-173.
[24] Koylu MZ, Asubay S, Yilmaz A. Determination of proton relaxivities of Mn(II), Cu(II) and Cr(III) added to solutions of serum proteins. Molecules 2009; 14: 1537-1545.
[25] Nofiele JT, Cheng HL. Ultrashort echo time for improved positive-contrast manganese-enhanced MRI of cancer. Plos One 2013; 8: e58617(1)-e58617(8).
[26] Delattre BM, Braunersreuther V, Hyacinthe JN, Crowe LA, Mach F, Vall´ee JP. Myocardial infarction quantification with manganese-enhanced MRI (MEMRI) in mice using a 3 T clinical scanner. NMR Biomed 2010; 23: 503-513.
[27] Bilgen M. Imaging corticospinal tract connectivity in injured rat spinal cord using manganese-enhanced MRI. BMC Med Imaging 2006; 6: 15(1)-15(8).
[28] Stikov N, Boudreau M, Levesque IR, Tardif CL, Barral JK, Pike GB. On the accuracy of T1 mapping: searching for common ground. Magn Reson Med 2014; 73: 514-522.
[29] Kingsley PB. Methods of measuring spin-lattice (T1) relaxation times: an annotated bibliography. Concept Magnetic Res 1999; 11: 243-276.
[30] Bloembergen N, Purcell EM, Pound RV. Relaxation effects in nuclear magnetic resonance absorption. Phys Rev 1948; 73: 679-712.
[31] Frank LR, Wong EC, Buxton RB. Slice profile effects in adiabatic inversion: application to multislice perfusion imaging. Magn Reson Med 1997; 38: 558-564.
[32] Barral JK, Gudmundson E, Stikov N, Amoli ME, Stoica P, Nishimura D. A robust methodology for in vivo T 1 mapping. Magn Reson Med 2010; 64: 1057-1067.
[33] Stanisz GJ, Odrobina EE, Pun J, Escaravage M, Graham SJ, Bronskill MJ, Henkelman RM. T1 , T2 relaxation and magnetization transfer in tissue at 3 T. Magn Reson Med 2005; 54: 507-512.
[34] Sharma P, Socolow J, Patel S, Pettigrew RI, Oshinski JN. Effect of Gd-DTPA-BMA on blood and myocardial T 1 at 1.5 T and 3 T in humans. J Magn Reson Imaging 2006; 23: 323-330.
[35] Park JY, Baek MJ, Choi ES, Woo S, Kim JH, Kim TJ, Kim TJ, Jung JC, Chae KS, Chang Y, Lee GH. Paramagnetic ultrasmall gadolinium oxide nanoparticles as advanced T1 MRI contrast agent: account for large longitudinal relaxivity, optimal particle diameter, and in vivo T1 MR images. Acs Nano 2009; 3: 3663-3669.
[36] Aime S, Fedeli F, Sanino A, Terreno E. A R2/R1 ratiometric procedure for a concentration-independent, pHresponsive, Gd(III)-based MRI agent. J Am Chem Soc 2006; 128: 11326-11327.
[37] Pan D, Senpan A, Caruthers SD, Williams TA, Scott MJ, Gaffney PJ, Wickline SA, Lanza GM. Sensitive and efficient detection of thrombus with fibrin-specific manganese nanocolloids. Chem Commun 2009; 22: 3234-3236.
[38] Cukur T, Santos JM, Pauly JM, Nishimura DG. Variable-density parallel imaging with partially localized coil sensitivities. IEEE T Med Imaging 2010; 29: 1173-1181.
[39] Cukur T, Santos JM, Nishimura DG, Pauly JM. Varying kernel-extent gridding reconstruction for undersampled variable-density spirals. Magn Reson Med 2008; 59: 196-201.
[40] Bishop C. Pattern Recognition and Machine Learning. New York, NY, USA: Springer-Verlag, 2006.
[41] Vehtari A, Gelman A, Gabry J. Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Arxiv 2016; 150704544v3.
[42] Rao CR, Wu Y. Linear model selection by cross-validation. J Stat Plan Infer 2005; 128: 231-240.
[43] Shao J. Linear model selection by cross-validation. J Am Stat Assoc 1993; 88: 486-494.
[44] Morgan LO, Nolle AW. Proton spin relaxation in aqueous solutions of paramagnetic ions. II. Cr+++, Mn++, Ni++, Cu++, and Gd+++. J Chem Phys 1959; 31: 365-368.
[45] Tofts PS. Quantitative MRI of the Brain: Measuring Changes Caused by Disease. West Sussex, UK: John Wiley & Sons Ltd., 2003.
[46] Caravan P, Farrar CT, Frullano L, Uppal R. Influence of molecular parameters and increasing magnetic field strength on relaxivity of gadolinium- and manganese-based T1 contrast agents. Contrast Media Mol I 2009; 4: 89-100.
[47] Kostopoulou A, Velu SKP, Thangavel K, Orsini F, Brintakis K, Psycharakis S, Ranella A, Bordonali L, Lappas A, Lascialfari A. Colloidal assemblies of oriented maghemite nanocrystals and their NMR relaxometric properties. Dalton T 2014; 43: 8395-8404.
[48] Roch A, Muller RN, Gillis P. Theory of proton relaxation induced by superparamagnetic particles. J Chem Phys 1999; 110: 5403-5411.
[49] Silva AC, Bock NA. Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophrenia Bull 2008; 34: 595-604.
[50] Pan D, Schmieder AH, Wickline SA, Lanza GM. Manganese-based MRI contrast agents: past, present, and future. Tetrahedron 2011; 67: 8431-8444.