Assessment of unilateral ureter obstruction with multi-parametric MRI
Corresponding Author
Feng Wang
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Correspondence to: Feng Wang, PhD, Vanderbilt University Institute of Imaging Science, AA-2105 MCN, 1161 21st Avenue South, Nashville, TN 37232, USA. E-mail: [email protected]Search for more papers by this authorKeiko Takahashi
Division of Nephrology and Hypertension, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorHua Li
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorZhongliang Zu
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorKe Li
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorJunzhong Xu
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorRaymond C. Harris
Division of Nephrology and Hypertension, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorTakamune Takahashi
Division of Nephrology and Hypertension, Vanderbilt University, Nashville, Tennessee, USA
These authors contributed equally to this work.
Search for more papers by this authorJohn C. Gore
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee, USA
These authors contributed equally to this work.
Search for more papers by this authorCorresponding Author
Feng Wang
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Correspondence to: Feng Wang, PhD, Vanderbilt University Institute of Imaging Science, AA-2105 MCN, 1161 21st Avenue South, Nashville, TN 37232, USA. E-mail: [email protected]Search for more papers by this authorKeiko Takahashi
Division of Nephrology and Hypertension, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorHua Li
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorZhongliang Zu
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorKe Li
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorJunzhong Xu
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorRaymond C. Harris
Division of Nephrology and Hypertension, Vanderbilt University, Nashville, Tennessee, USA
Search for more papers by this authorTakamune Takahashi
Division of Nephrology and Hypertension, Vanderbilt University, Nashville, Tennessee, USA
These authors contributed equally to this work.
Search for more papers by this authorJohn C. Gore
Vanderbilt University Institute of Imaging Science, Nashville, Tennessee, USA
Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, Tennessee, USA
Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee, USA
These authors contributed equally to this work.
Search for more papers by this authorAbstract
Purpose
Quantitative multi-parametric MRI (mpMRI) methods may allow the assessment of renal injury and function in a sensitive and objective manner. This study aimed to evaluate an array of MRI methods that exploit endogenous contrasts including relaxation rates, pool size ratio (PSR) derived from quantitative magnetization transfer (qMT), chemical exchange saturation transfer (CEST), nuclear Overhauser enhancement (NOE), and apparent diffusion coefficient (ADC) for their sensitivity and specificity in detecting abnormal features associated with kidney disease in a murine model of unilateral ureter obstruction (UUO).
Methods
MRI scans were performed in anesthetized C57BL/6N mice 1, 3, or 6 days after UUO at 7T. Paraffin tissue sections were stained with Masson trichrome following MRI.
Results
Compared to contralateral kidneys, the cortices of UUO kidneys showed decreases of relaxation rates R1 and R2, PSR, NOE, and ADC. No significant changes in CEST effects were observed for the cortical region of UUO kidneys. The MRI parametric changes in renal cortex are related to tubular cell death, tubular atrophy, tubular dilation, urine retention, and interstitial fibrosis in the cortex of UUO kidneys.
Conclusion
Measurements of multiple MRI parameters provide comprehensive information about the molecular and cellular changes produced by UUO. Magn Reson Med 79:2216–2227, 2018. © 2017 International Society for Magnetic Resonance in Medicine.
Supporting Information
Additional supporting information may be found in the online version of this article.
| Filename | Description |
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| mrm26849-sup-0001-suppfigs.docx2.1 MB |
Fig. S1. Representative CEST images collected at different RF offsets. Fig. S2. Representative raw qMT data. Fig. S3. Comparison of cortical CEST effects at 1.2 ppm RF offset between CL and UUO kidneys 6 days after UUO surgery (n = 8). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Collins AJ, Foley R, Herzog C, et al. Excerpts from the United States Renal Data System 2007 annual data report. Am J Kidney Dis 2008; 51(Suppl 1): S1–S320.
- 2 Cochrane AL, Kett MM, Samuel CS, Campanale NV, Anderson WP, Hume DA, Little MH, Bertram JF, Ricardo SD. Renal structural and functional repair in a mouse model of reversal of ureteral obstruction. J Am Soc Nephrol 2005; 16: 3623–3630.
- 3 Pat B, Yang T, Kong C, Watters D, Johnson DW, Gobe G. Activation of ERK in renal fibrosis after unilateral ureteral obstruction: modulation by antioxidants. Kidney Int 2005; 67: 931–943.
- 4 Wang F, Jiang R, Takahashi K, Gore J, Harris RC, Takahashi T, Quarles CC. Longitudinal assessment of mouse renal injury using high-resolution anatomic and magnetization transfer MR imaging. Magn Reson Imaging 2014; 32: 1125–1132.
- 5 Togao O, Doi S, Kuro-o M, Masaki T, Yorioka N, Takahashi M. Assessment of renal fibrosis with diffusion-weighted MR imaging: study with murine model of unilateral ureteral obstruction. Radiology 2010; 255: 772–780.
- 6 Michaely HJ, Sourbron S, Dietrich O, Attenberger U, Reiser MF, Schoenberg SO. Functional renal MR imaging: an overview. Abdom Imaging 2007; 32: 758–771.
- 7 Takahashi T, Wang F, Quarles CC. Current MRI techniques for the assessment of renal disease. Curr Opin Nephrol Hypertens 2015; 24: 217–223.
- 8 Xie L, Bennett KM, Liu C, Johnson GA, Zhang JL, Lee VS. MRI tools for assessment of microstructure and nephron function of the kidney. Am J Physiol Renal Physiol 2016; 311: F1109–F1124.
- 9 Niendorf T, Pohlmann A, Arakelyan K, et al. How bold is blood oxygenation level-dependent (BOLD) magnetic resonance imaging of the kidney? Opportunities, challenges and future directions. Acta Physiol 2015; 213: 19–38.
- 10 Pohlmann A, Arakelyan K, Hentschel J, Cantow K, Flemming B, Ladwig M, Waiczies S, Seeliger E, Niendorf T. Detailing the relation between renal T2* and renal tissue pO2 using an integrated approach of parametric magnetic resonance imaging and invasive physiological measurements. Invest Radiol 2014; 49: 547–560.
- 11 Zhang JL, Rusinek H, Chandarana H, Lee VS. Functional MRI of the kidneys. J Magn Reson Imaging 2013; 37: 282–293.
- 12 Kobayashi H, Jo SK, Kawamoto S, Yasuda H, Hu X, Knopp MV, Brechbiel MW, Choyke PL, Star RA. Polyamine dendrimer-based MRI contrast agents for functional kidney imaging to diagnose acute renal failure. J Magn Reson Imaging 2004; 20: 512–518.
- 13 Wang F, Jiang RT, Tantawy MN, Borza DB, Takahashi K, Gore JC, Harris RC, Takahashi T, Quarles CC. Repeatability and sensitivity of high resolution blood volume mapping in mouse kidney disease. J Magn Reson Imaging 2014; 39: 866–871.
- 14 Dear JW, Kobayashi H, Brechbiel MW, Star RA. Imaging acute renal failure with polyamine dendrimer-based MRI contrast agents. Nephron Clin Pract 2006; 103: c45–c49.
- 15 Perazella MA. Current status of gadolinium toxicity in patients with kidney disease. Clin J Am Soc Nephrol 2009; 4: 461–469.
- 16 Prasad P, Li LP, Halter S, Cabray J, Ye M, Batlle D. Evaluation of renal hypoxia in diabetic mice by BOLD MRI. Invest Radiol 2010; 45: 819–822.
- 17 Mounier-Vehier C, Lions C, Devos P, Jaboureck O, Willoteaux S, Carre A, Beregi JP. Cortical thickness: an early morphological marker of atherosclerotic renal disease. Kidney Int 2002; 61: 591–598.
- 18 Wolff SD, Balaban RS. Magnetization transfer contrast (MTC) and tissue water proton relaxation in vivo. Magn Reson Med 1989; 10: 135–144.
- 19 Henkelman RM, Stanisz GJ, Graham SJ. Magnetization transfer in MRI: a review. NMR Biomed 2001; 14: 57–64.
- 20 Adler J, Swanson SD, Schmiedlin-Ren P, Higgins PD, Golembeski CP, Polydorides AD, McKenna BJ, Hussain HK, Verrot TM, Zimmermann EM. Magnetization transfer helps detect intestinal fibrosis in an animal model of Crohn disease. Radiology 2011; 259: 127–135.
- 21 Wang F, Li K, Mishra A, Gochberg D, Min Chen L, Gore JC. Longitudinal assessment of spinal cord injuries in nonhuman primates with quantitative magnetization transfer. Magn Reson Med 2016; 75: 1685–1696.
- 22 Bailey C, Desmond KL, Czarnota GJ, Stanisz GJ. Quantitative magnetization transfer studies of apoptotic cell death. Magn Reson Med 2011; 66: 264–269.
- 23 Bosch CS, Ackerman JJH, Tilton RG, Shalwitz RA. In vivo NMR imaging and spectroscopic investigation of renal pathology in lean and obese rat kidneys. Magn Reson Med 1993; 29: 335–344.
- 24 Kline TL, Irazabal MV, Ebrahimi B, et al. Utilizing magnetization transfer imaging to investigate tissue remodeling in a murine model of autosomal dominant polycystic kidney disease. Magn Reson Med 2016; 75: 1466–1473.
- 25 Henkelman RM, Huang X, Xiang QS, Stanisz GJ, Swanson SD, Bronskill MJ. Quantitative interpretation of magnetization transfer. Magn Reson Med 1993; 29: 759–766.
- 26 Sled JG, Pike GB. Quantitative interpretation of magnetization transfer in spoiled gradient echo MRI sequences. J Magn Reson 2000; 145: 24–36.
- 27 Gochberg DF, Gore JC. Quantitative imaging of magnetization transfer using an inversion recovery sequence. Magn Reson Med 2003; 49: 501–505.
- 28 Zhou JY, Blakeley JO, Hua J, Kim M, Laterra J, Pomper MG, van Zijl PCM. Practical data acquisition method for human brain tumor amide proton transfer (APT) imaging. Magn Reson Med 2008; 60: 842–849.
- 29 Wang F, Qi HX, Zu Z, Mishra A, Tang C, Gore JC, Chen LM. Multiparametric MRI reveals dynamic changes in molecular signatures of injured spinal cord in monkeys. Magn Reson Med 2015; 74: 1125–1137.
- 30 Wang F, Zu Z, Wu R, Wu TL, Gore JC, Chen LM. MRI evaluation of regional and longitudinal changes in Z-spectra of injured spinal cord of monkeys. Magn Reson Med 2018; 79: 1070–1082.
- 31 Sun PZ, Sorensen AG. Imaging pH using the chemical exchange saturation transfer (CEST) MRI: correction of concomitant RF irradiation effects to quantify CEST MRI for chemical exchange rate and pH. Magn Reson Med 2008; 60: 390–397.
- 32 Jin T, Wang P, Zong XP, Kim SG. MR imaging of the amide-proton transfer effect and the pH-insensitive nuclear overhauser effect at 9.4 T. Magn Reson Med 2013; 69: 760–770.
- 33 van Zijl PC, Jones CK, Ren J, Malloy CR, Sherry AD. MRI detection of glycogen in vivo by using chemical exchange saturation transfer imaging (glycoCEST). Proc Natl Acad Sci USA 2007; 104: 4359–4364.
- 34 Ren JM, Marshall BA, Gulve EA, Gao JP, Johnson DW, Holloszy JO, Mueckler M. Evidence from transgenic mice that glucose-transport is rate-limiting for glycogen deposition and glycolysis in skeletal-muscle. J Biol Chem 1993; 268: 16113–16115.
- 35 Wang F, Kopylov D, Zu Z, Takahashi K, Wang S, Quarles CC, Gore JC, Harris RC, Takahashi T. Mapping murine diabetic kidney disease using chemical exchange saturation transfer MRI. Magn Reson Med 2016; 75: 1685–1695.
- 36 Longo DL, Busato A, Lanzardo S, Antico F, Aime S. Imaging the pH evolution of an acute kidney injury model by means of iopamidol, a MRI-CEST pH-responsive contrast agent. Magn Reson Med 2013; 70: 859–864.
- 37 Zhang XY, Wang F, Afzal A, Xu JZ, Gore JC, Gochberg DF, Zu ZL. A new NOE-mediated MT signal at around-1.6 ppm for detecting ischemic stroke in rat brain. Magn Reson Imaging 2016; 34: 1100–1106.
- 38 Zhang XY, Wang F, Jin T, Xu J, Xie J, Gochberg DF, Gore JC, Zu Z. MR imaging of a novel NOE-mediated magnetization transfer with water in rat brain at 9.4 T. Magn Reson Med 2017; 78: 588–597.
- 39 Pluim JPW, Maintz JBA, Viergever MA. Mutual-information-based registration of medical images: a survey. IEEE Trans Med Imaging 2003; 22: 986–1004.
- 40 Bane O, Wagner M, Zhang JL, Dyvorne HA, Orton M, Rusinek H, Taouli B. Assessment of renal function using intravoxel incoherent motion diffusion-weighted imaging and dynamic contrast-enhanced MRI. J Magn Reson Imaging 2016; 44: 317–326.
- 41 Smith SA, Edden RA, Farrell JA, Barker PB, Van Zijl PC. Measurement of T1 and T2 in the cervical spinal cord at 3 tesla. Magn Reson Med 2008; 60: 213–219.
- 42 Ramani A, Dalton C, Miller DH, Tofts PS, Barker GJ. Precise estimate of fundamental in-vivo MT parameters in human brain in clinically feasible times. Magn Reson Imaging 2002; 20: 721–731.
- 43 Desmond KL, Moosvi F, Stanisz GJ. Mapping of amide, amine, and aliphatic peaks in the CEST spectra of murine xenografts at 7 T. Magn Reson Med 2014; 71: 1841–1853.
- 44 Tantawy MN, Jiang R, Wang F, et al. Assessment of renal function in mice with unilateral ureteral obstruction using 99mTc-MAG3 dynamic scintigraphy. BMC Nephrol 2012; 13: 168.
- 45 Jonas J, Winter R, Grandinetti PJ, Driscoll D. High-pressure 2D NOESY experiments on phospholipid-vesicles. J Magn Reson 1990; 87: 536–547.
- 46 Janve VA, Zu Z, Yao SY, Li K, Zhang FL, Wilson KJ, Ou X, Does MD, Subramaniam S, Gochberg DF. The radial diffusivity and magnetization transfer pool size ratio are sensitive markers for demyelination in a rat model of type III multiple sclerosis (MS) lesions. Neuroimage 2013; 74: 298–305.
