Multiparametric Renal Magnetic Resonance Imaging: Validation, Interventions, and Alterations in Chronic Kidney Disease

Eleanor F Cox, Charlotte E Buchanan, Christopher R Bradley, Benjamin Prestwich, Huda Mahmoud, Maarten Taal, Nicholas M Selby, Susan T Francis, Eleanor F Cox, Charlotte E Buchanan, Christopher R Bradley, Benjamin Prestwich, Huda Mahmoud, Maarten Taal, Nicholas M Selby, Susan T Francis

Abstract

Background: This paper outlines a multiparametric renal MRI acquisition and analysis protocol to allow non-invasive assessment of hemodynamics (renal artery blood flow and perfusion), oxygenation (BOLD T2*), and microstructure (diffusion, T1 mapping). Methods: We use our multiparametric renal MRI protocol to provide (1) a comprehensive set of MRI parameters [renal artery and vein blood flow, perfusion, T1, T2*, diffusion (ADC, D, D*, fp), and total kidney volume] in a large cohort of healthy participants (127 participants with mean age of 41 ± 19 years) and show the MR field strength (1.5 T vs. 3 T) dependence of T1 and T2* relaxation times; (2) the repeatability of multiparametric MRI measures in 11 healthy participants; (3) changes in MRI measures in response to hypercapnic and hyperoxic modulations in six healthy participants; and (4) pilot data showing the application of the multiparametric protocol in 11 patients with Chronic Kidney Disease (CKD). Results: Baseline measures were in-line with literature values, and as expected, T1-values were longer at 3 T compared with 1.5 T, with increased T1 corticomedullary differentiation at 3 T. Conversely, T2* was longer at 1.5 T. Inter-scan coefficients of variation (CoVs) of T1 mapping and ADC were very good at <2.9%. Intra class correlations (ICCs) were high for cortex perfusion (0.801), cortex and medulla T1 (0.848 and 0.997 using SE-EPI), and renal artery flow (0.844). In response to hypercapnia, a decrease in cortex T2* was observed, whilst no significant effect of hyperoxia on T2* was found. In CKD patients, renal artery and vein blood flow, and renal perfusion was lower than for healthy participants. Renal cortex and medulla T1 was significantly higher in CKD patients compared to healthy participants, with corticomedullary T1 differentiation reduced in CKD patients compared to healthy participants. No significant difference was found in renal T2*. Conclusions: Multiparametric MRI is a powerful technique for the assessment of changes in structure, hemodynamics, and oxygenation in a single scan session. This protocol provides the potential to assess the pathophysiological mechanisms in various etiologies of renal disease, and to assess the efficacy of drug treatments.

Keywords: arterial spin labeling; hemodynamics; magnetic resonance imaging; oxygenation; renal function.

Figures

Figure 1
Figure 1
Multiparametric non-invasive renal MRI protocol.
Figure 2
Figure 2
Modified respiratory triggered inversion recovery sequence shown for (A) short (TI1) and (B) long (TI2) inversion time. By altering the variable delay, Tv, each image acquisition is collected at a constant time (Tv + TI) following the respiratory trigger. First arrow indicates the respiratory trigger (“Respiratory Trigger”), second the inversion pulse (“Inversion”), and the shaded block indicates the image acquisition readout (“Acquisition”).
Figure 3
Figure 3
(A) Example image analysis for a healthy participant indicating segmentation of the kidneys from the T1 map, definition of cortex and medulla masks from the histogram, and the application of the renal cortex mask to an arterial spin labeling perfusion map allowing the interrogation of a histogram [for mode and full-width-at-half-maximum (FWHM)] of renal cortex perfusion values. (B) Example image analysis for a chronic kidney disease patient indicating definition of cortex and medulla masks from the T1 histogram of the kidneys.
Figure 4
Figure 4
Example arterial spin labeling perfusion, longitudinal relaxation time T1, ADC (apparent diffusion coefficient), and transverse relaxation time T2* maps in a healthy participant.
Figure 5
Figure 5
The mode and FWHM (full-width-at-half-maximum) in the renal cortex and medulla of healthy participants for (A) transverse relaxation time T2* during normoxia, hyperoxia, and hypercapnia; (B) longitudinal relaxation time T1 during normoxia and hyperoxia.

References

    1. Adler S., Huang H., Wolin M. S., Kaminski P. M. (2004). Oxidant stress leads to impaired regulation of renal cortical oxygen consumption by nitric oxide in the aging kidney. J. Am. Soc. Nephrol. 15, 52–60. 10.1097/01.ASN.0000101032.21097.C5
    1. Artz N. S., Sadowski E. A., Wentland A. L., Djamali A., Grist T. M., Seo S., et al. . (2011a). Reproducibility of renal perfusion MR imaging in native and transplanted kidneys using non-contrast arterial spin labeling. J. Magn. Reson. Imaging 33, 1414–1421. 10.1002/jmri.22552
    1. Artz N. S., Sadowski E. A., Wentland A. L., Grist T. M., Seo S., Djamali A., et al. . (2011b). Arterial spin labeling MRI for assessment of perfusion in native and transplanted kidneys. Magn. Reson. Imaging 29, 74–82. 10.1016/j.mri.2010.07.018
    1. Bax L., Bakker C. J., Klein W. M., Blanken N., Beutler J. J., Mali W. P. (2005). Renal blood flow measurements with use of phase-contrast magnetic resonance imaging: normal values and reproducibility. J. Vasc. Intervent. Radiol. 16, 807–814. 10.1097/01.RVI.0000161144.98350.28
    1. Becker H. F., Polo O., McNamara S. G., Berthon-Jones M., Sullivan C. E. (1996). Effect of different levels of hyperoxia on breathing in healthy subjects. J. Appl. Physiol. 81, 1683–1690.
    1. Blantz R. C., Deng A., Miracle C. M., Thomson S. C. (2007). Regulation of kidney function and metabolism: a question of supply and demand. Trans. Am. Clin. Climatol. Assoc. 118, 23–43.
    1. Boss A., Martirosian P., Graf H., Claussen C. D., Schlemmer H. P., Schick F. (2005). High resolution MR perfusion imaging of the kidneys at 3 Tesla without administration of contrast media. RoFo 177, 1625–1630. 10.1055/s-2005-858761
    1. Buchanan C. E., Cox E. F., Francis S. T. (eds.). (2015). Evaluation of Readout Schemes for Arterial Spin Labelling in the Human Kidney. Toronto, ON: Int Soc Mag Reson.
    1. Buxton R. B., Frank L. R., Wong E. C., Siewert B., Warach S., Edelman R. R. (1998). A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn. Reson. Med. 40, 383–396. 10.1002/mrm.1910400308
    1. Chowdhury A. H., Cox E. F., Francis S. T., Lobo D. N. (2012). A randomized, controlled, double-blind crossover study on the effects of 2-L infusions of 0.9% saline and plasma-lyte(R) 148 on renal blood flow velocity and renal cortical tissue perfusion in healthy volunteers. Ann. Surg. 256, 18–24. 10.1097/SLA.0b013e318256be72
    1. Cohen E. I., Kelly S. A., Edye M., Mitty H. A., Bromberg J. S. (2009). MRI estimation of total renal volume demonstrates significant association with healthy donor weight. Eur. J. Radiol. 71, 283–287. 10.1016/j.ejrad.2008.03.006
    1. Cutajar M., Clayden J. D., Clark C. A., Gordon I. (2011). Test-retest reliability and repeatability of renal diffusion tensor MRI in healthy subjects. Eur. J. Radiol. 80, e263–e268. 10.1016/j.ejrad.2010.12.018
    1. Cutajar M., Thomas D. L., Banks T., Clark C. A., Golay X., Gordon I. (2012). Repeatability of renal arterial spin labelling MRI in healthy subjects. Magma 25, 145–153. 10.1007/s10334-011-0300-9
    1. Cutajar M., Thomas D. L., Hales P. W., Banks T., Clark C. A., Gordon I. (2014). Comparison of ASL and DCE MRI for the non-invasive measurement of renal blood flow: quantification and reproducibility. Eur. Radiol. 24, 1300–1308. 10.1007/s00330-014-3130-0
    1. Dambreville S., Chapman A. B., Torres V. E., King B. F., Wallin A. K., Frakes D. H., et al. . (2010). Renal arterial blood flow measurement by breath-held MRI: accuracy in phantom scans and reproducibility in healthy subjects. Magn. Reson. Med. 63, 940–950. 10.1002/mrm.22278
    1. de Bazelaire C. M., Duhamel G. D., Rofsky N. M., Alsop D. C. (2004). MR imaging relaxation times of abdominal and pelvic tissues measured in vivo at 3.0 T: preliminary results. Radiology 230, 652–659. 10.1148/radiol.2303021331
    1. Debatin J. F., Ting R. H., Wegmuller H., Sommer F. G., Fredrickson J. O., Brosnan T. J., et al. . (1994). Renal artery blood flow: quantitation with phase-contrast MR imaging with and without breath holding. Radiology 190, 371–378. 10.1148/radiology.190.2.8284383
    1. Ding J., Xing W., Wu D., Chen J., Pan L., Sun J., et al. (2015). Evaluation of renal oxygenation level changes after water loading using susceptibility-weighted imaging and T2* mapping. Korean J. Radiol. 16, 827–834. 10.3348/kjr.2015.16.4.827
    1. Ding Y., Mason R. P., McColl R. W., Yuan Q., Hallac R. R., Sims R. D., et al. . (2013). Simultaneous measurement of tissue oxygen level-dependent (TOLD) and blood oxygenation level-dependent (BOLD) effects in abdominal tissue oxygenation level studies. J. Magn. Reson. Imaging 38, 1230–1236. 10.1002/jmri.24006
    1. Dobre M. C., Ugurbil K., Marjanska M. (2007). Determination of blood longitudinal relaxation time (T1) at high magnetic field strengths. Magn. Reson. Imaging 25, 733–735. 10.1016/j.mri.2006.10.020
    1. Donati O. F., Nanz D., Serra A. L., Boss A. (2012). Quantitative BOLD response of the renal medulla to hyperoxic challenge at 1.5 T and 3.0 T. NMR Biomed. 25, 1133–1138. 10.1002/nbm.2781
    1. Dong J., Yang L., Su T., Yang X., Chen B., Zhang J., et al. . (2013). Quantitative assessment of acute kidney injury by noninvasive arterial spin labeling perfusion MRI: a pilot study. Sci. China Life Sci. 56, 745–750. 10.1007/s11427-013-4503-3
    1. Epstein F. H., Prasad P. (2000). Effects of furosemide on medullary oxygenation in younger and older subjects. Kidney Int. 57, 2080–2083. 10.1046/j.1523-1755.2000.00057.x
    1. Evans R. G., Gardiner B. S., Smith D. W., O'Connor P. M. (2008). Intrarenal oxygenation: unique challenges and the biophysical basis of homeostasis. Am. J. Physiol. Renal Physiol. 295, F1259–F1270. 10.1152/ajprenal.90230.2008
    1. Fenchel M., Martirosian P., Langanke J., Giersch J., Miller S., Stauder N. I., et al. . (2006). Perfusion MR imaging with FAIR true FISP spin labeling in patients with and without renal artery stenosis: initial experience. Radiology 238, 1013–1021. 10.1148/radiol.2382041623
    1. Friedli I., Crowe L. A., Berchtold L., Moll S., Hadaya K., de Perrot T., et al. . (2016). New Magnetic resonance imaging index for renal fibrosis assessment: a comparison between diffusion-weighted imaging and T1 mapping with histological validation. Sci. Rep. 6:30088. 10.1038/srep30088
    1. Ganesh T., Estrada M., Duffin J., Cheng H. L. (2016). T2* and T1 assessment of abdominal tissue response to graded hypoxia and hypercapnia using a controlled gas mixing circuit for small animals. J. Magn. Reson. Imaging 44, 305–316. 10.1002/jmri.25169
    1. Gardener A. G., Francis S. T. (2010). Multislice perfusion of the kidneys using parallel imaging: image acquisition and analysis strategies. Magn. Reson. Med. 63, 1627–1636. 10.1002/mrm.22387
    1. Gillis K. A., McComb C., Foster J. E., Taylor A. H., Patel R. K., Morris S. T., et al. . (2014). Inter-study reproducibility of arterial spin labelling magnetic resonance imaging for measurement of renal perfusion in healthy volunteers at 3 Tesla. BMC Nephrol. 15:23. 10.1186/1471-2369-15-23
    1. Gillis K. A., McComb C., Patel R. K., Stevens K. K., Schneider M. P., Radjenovic A., et al. . (2016). Non-contrast renal magnetic resonance imaging to assess perfusion and corticomedullary differentiation in health and chronic kidney disease. Nephron 133, 183–192. 10.1159/000447601
    1. Goyal A., Sharma R., Bhalla A. S., Gamanagatti S., Seth A. (2012). Diffusion-weighted MRI in assessment of renal dysfunction. Indian J. Radiol. Imaging 22, 155–159. 10.4103/0971-3026.107169
    1. Hammon M., Janka R., Siegl C., Seuss H., Grosso R., Martirosian P., et al. . (2016). Reproducibility of kidney perfusion measurements with arterial spin labeling at 1.5 Tesla MRI combined with semiautomatic segmentation for differential cortical and medullary assessment. Medicine 95:e3083. 10.1097/MD.0000000000003083
    1. Heusch P., Wittsack H. J., Heusner T., Buchbender C., Quang M. N., Martirosian P., et al. . (2013). Correlation of biexponential diffusion parameters with arterial spin-labeling perfusion MRI: results in transplanted kidneys. Invest. Radiol. 48, 140–144. 10.1097/RLI.0b013e318277bfe3
    1. Hoad C. L., Palaniyappan N., Kaye P., Chernova Y., James M. W., Costigan C., et al. (2015). A study of T(1) relaxation time as a measure of liver fibrosis and the influence of confounding histological factors. NMR Biomed. 28, 706–714. 10.1002/nbm.3299
    1. Iles L., Pfluger H., Phrommintikul A., Cherayath J., Aksit P., Gupta S. N., et al. . (2008). Evaluation of diffuse myocardial fibrosis in heart failure with cardiac magnetic resonance contrast-enhanced T1 mapping. J. Am. Coll. Cardiol. 52, 1574–1580. 10.1016/j.jacc.2008.06.049
    1. Inoue T., Kozawa E., Okada H., Inukai K., Watanabe S., Kikuta T., et al. . (2011). Noninvasive evaluation of kidney hypoxia and fibrosis using magnetic resonance imaging. J. Am. Soc. Nephrol. 22, 1429–1434. 10.1681/ASN.2010111143
    1. Jellis C. L., Kwon D. H. (2014). Myocardial T1 mapping: modalities and clinical applications. Cardiovasc. Diagn. Ther. 4, 126–137. 10.3978/j.issn.2223-3652.2013.09.03
    1. Jones R. A., Ries M., Moonen C. T., Grenier N. (2002). Imaging the changes in renal T1 induced by the inhalation of pure oxygen: a feasibility study. Magn. Reson. Med. 47, 728–735. 10.1002/mrm.10127
    1. Karger N., Biederer J., Lusse S., Grimm J., Steffens J., Heller M., et al. . (2000). Quantitation of renal perfusion using arterial spin labeling with FAIR-UFLARE. Magn. Reson. Imaging 18, 641–647. 10.1016/S0730-725X(00)00155-7
    1. Khatir D. S., Pedersen M., Jespersen B., Buus N. H. (2014). Reproducibility of MRI renal artery blood flow and BOLD measurements in patients with chronic kidney disease and healthy controls. J. Magn. Reson. Imaging 40, 1091–1098. 10.1002/jmri.24446
    1. Khatir D. S., Pedersen M., Jespersen B., Buus N. H. (2015). Evaluation of renal blood flow and oxygenation in CKD using magnetic resonance imaging. Am. J. Kidney Dis. 66, 402–411. 10.1053/j.ajkd.2014.11.022
    1. Kiefer C., Schroth G., Gralla J., Diehm N., Baumgartner I., Husmann M. (2009). A feasibility study on model-based evaluation of kidney perfusion measured by means of FAIR prepared true-FISP arterial spin labeling (ASL) on a 3-T MR scanner. Acad. Radiol. 16, 79–87. 10.1016/j.acra.2008.04.024
    1. Koh D. M., Collins D. J., Orton M. R. (2011). Intravoxel incoherent motion in body diffusion-weighted MRI: reality and challenges. Am. J. Roentgenol. 196, 1351–1361. 10.2214/AJR.10.5515
    1. Le Bihan D., Breton E., Lallemand D., Aubin M. L., Vignaud J., Laval-Jeantet M. (1988). Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168, 497–505. 10.1148/radiology.168.2.3393671
    1. Li L. P., Storey P., Pierchala L., Li W., Polzin J., Prasad P. (2004a). Evaluation of the reproducibility of intrarenal R2* and DeltaR2* measurements following administration of furosemide and during waterload. J. Magn. Reson. Imaging 19, 610–616. 10.1002/jmri.20043
    1. Li L. P., Vu A. T., Li B. S., Dunkle E., Prasad P. V. (2004b). Evaluation of intrarenal oxygenation by BOLD MRI at 3.0 T. J. Magn. Reson. Imaging 20, 901–904. 10.1002/jmri.20176
    1. Maril N., Margalit R., Rosen S., Heyman S. N., Degani H. (2006). Detection of evolving acute tubular necrosis with renal 23Na MRI: studies in rats. Kidney Int. 69, 765–768. 10.1038/sj.ki.5000152
    1. Martirosian P., Klose U., Mader I., Schick F. (2004). FAIR true-FISP perfusion imaging of the kidneys. Magn. Reson. Med. 51, 353–361. 10.1002/mrm.10709
    1. Michaely H. J., Metzger L., Haneder S., Hansmann J., Schoenberg S. O., Attenberger U. I. (2012). Renal BOLD-MRI does not reflect renal function in chronic kidney disease. Kidney Int. 81, 684–689. 10.1038/ki.2011.455
    1. Michaely H. J., Schoenberg S. O., Ittrich C., Dikow R., Bock M., Guenther M. (2004). Renal disease: value of functional magnetic resonance imaging with flow and perfusion measurements. Invest. Radiol. 39, 698–705. 10.1097/00004424-200411000-00008
    1. Milani B., Ansaloni A., Sousa-Guimaraes S., Vakilzadeh N., Piskunowicz M., Vogt B., et al. . (2016). Reduction of cortical oxygenation in chronic kidney disease: evidence obtained with a new analysis method of blood oxygenation level-dependent magnetic resonance imaging. Nephrol. Dial. Transplant. [Epub ahead of print]. 10.1093/ndt/gfw362
    1. Milman Z., Heyman S. N., Corchia N., Edrei Y., Axelrod J. H., Rosenberger C., et al. . (2013). Hemodynamic response magnetic resonance imaging: application for renal hemodynamic characterization. Nephrol. Dial. Transplant. 28, 1150–1156. 10.1093/ndt/gfs541
    1. Mozes F. E., Tunnicliffe E. M., Pavlides M., Robson M. D. (2016). Influence of fat on liver T1 measurements using modified Look-Locker inversion recovery (MOLLI) methods at 3T. J. Magn. Reson. Imaging 44, 105–111. 10.1002/jmri.25146
    1. Niendorf T., Pohlmann A., Arakelyan K., Flemming B., Cantow K., Hentschel J., et al. . (2015). How bold is blood oxygenation level-dependent (BOLD) magnetic resonance imaging of the kidney? Opportunities, challenges and future directions. Acta Physiol. 213, 19–38. 10.1111/apha.12393
    1. Niles D. J., Artz N. S., Djamali A., Sadowski E. A., Grist T. M., Fain S. B. (2016). Longitudinal assessment of renal perfusion and oxygenation in transplant donor-recipient pairs using arterial spin labeling and blood oxygen level-dependent magnetic resonance imaging. Invest. Radiol. 51, 113–120. 10.1097/RLI.0000000000000210
    1. Notohamiprodjo M., Chandarana H., Mikheev A., Rusinek H., Grinstead J., Feiweier T., et al. . (2015). Combined intravoxel incoherent motion and diffusion tensor imaging of renal diffusion and flow anisotropy. Magn. Reson. Med. 73, 1526–1532. 10.1002/mrm.25245
    1. O'Connor J. P., Jackson A., Buonaccorsi G. A., Buckley D. L., Roberts C., Watson Y., et al. . (2007). Organ-specific effects of oxygen and carbogen gas inhalation on tissue longitudinal relaxation times. Magn. Reson. Med. 58, 490–496. 10.1002/mrm.21357
    1. O'Connor J. P., Naish J. H., Jackson A., Waterton J. C., Watson Y., Cheung S., et al. (2009). Comparison of normal tissue R1 and R2* modulation by oxygen and carbogen. Magn. Reson. Med. 61, 75–83. 10.1002/mrm.21815
    1. Park J. B., Santos J. M., Hargreaves B. A., Nayak K. S., Sommer G., Hu B. S., et al. . (2005). Rapid measurement of renal artery blood flow with ungated spiral phase-contrast MRI. J. Magn. Reson. Imaging 21, 590–595. 10.1002/jmri.20325
    1. Park S. H., Wang D. J., Duong T. Q. (2013). Balanced steady state free precession for arterial spin labeling MRI: initial experience for blood flow mapping in human brain, retina, and kidney. Magn. Reson. Imaging 31, 1044–1050. 10.1016/j.mri.2013.03.024
    1. Park S. Y., Kim C. K., Park B. K., Huh W., Kim S. J., Kim B. (2012). Evaluation of transplanted kidneys using blood oxygenation level-dependent MRI at 3 T: a preliminary study. Am. J. Roentgenol. 198, 1108–1114. 10.2214/AJR.11.7253
    1. Piskunowicz M., Hofmann L., Zuercher E., Bassi I., Milani B., Stuber M., et al. . (2015). A new technique with high reproducibility to estimate renal oxygenation using BOLD-MRI in chronic kidney disease. Magn. Reson. Imaging 33, 253–261. 10.1016/j.mri.2014.12.002
    1. Prasad P. V., Epstein F. H. (1999). Changes in renal medullary pO2 during water diuresis as evaluated by blood oxygenation level-dependent magnetic resonance imaging: effects of aging and cyclooxygenase inhibition. Kidney Int. 55, 294–298. 10.1046/j.1523-1755.1999.00237.x
    1. Prasad P. V., Edelman R. R., Epstein F. H. (1996). Noninvasive evaluation of intrarenal oxygenation with BOLD MRI. Circulation 94, 3271–3275. 10.1161/01.CIR.94.12.3271
    1. Pruijm M., Hofmann L., Piskunowicz M., Muller M. E., Zweiacker C., Bassi I., et al. . (2014). Determinants of renal tissue oxygenation as measured with BOLD-MRI in chronic kidney disease and hypertension in humans. PLoS ONE 9:e95895. 10.1371/journal.pone.0095895
    1. Pruijm M., Milani B., Burnier M. (2017). Blood oxygenation level-dependent MRI to assess renal oxygenation in renal diseases: progresses and challenges. Front. Physiol. 7:667. 10.3389/fphys.2016.00667
    1. Ritt M., Janka R., Schneider M. P., Martirosian P., Hornegger J., Bautz W., et al. . (2010). Measurement of kidney perfusion by magnetic resonance imaging: comparison of MRI with arterial spin labeling to para-aminohippuric acid plasma clearance in male subjects with metabolic syndrome. Nephrol. Dial. 25, 1126–1133. 10.1093/ndt/gfp639
    1. Rossi C., Artunc F., Martirosian P., Schlemmer H. P., Schick F., Boss A. (2012). Histogram analysis of renal arterial spin labeling perfusion data reveals differences between volunteers and patients with mild chronic kidney disease. Invest. Radiol. 47, 490–496. 10.1097/RLI.0b013e318257063a
    1. Schmitt P., Griswold M. A., Jakob P. M., Kotas M., Gulani V., Flentje M., et al. (2004). Inversion recovery TrueFISP: quantification of T1, T2, and spin density. Magn. Reson. Med. 51, 661–667. 10.1002/mrm.20058
    1. Schoenberg S. O., Just A., Bock M., Knopp M. V., Persson P. B., Kirchheim H. R. (1997). Noninvasive analysis of renal artery blood flow dynamics with MR cine phase-contrast flow measurements. Am. J. Physiol. 272, H2477–H2484.
    1. Seuss H., Janka R., Prummer M., Cavallaro A., Hammon R., Theis R., et al. . (2017). Development and evaluation of a semi-automated segmentation tool and a modified ellipsoid formula for volumetric analysis of the kidney in non-contrast T2-weighted MR images. J. Digit. Imaging 30, 244–254. 10.1007/s10278-016-9936-3
    1. Sigmund E. E., Vivier P. H., Sui D., Lamparello N. A., Tantillo K., Mikheev A., et al. . (2012). Intravoxel incoherent motion and diffusion-tensor imaging in renal tissue under hydration and furosemide flow challenges. Radiology 263, 758–769. 10.1148/radiol.12111327
    1. Simon-Zoula S. C., Hofmann L., Giger A., Vogt B., Vock P., Frey F. J., et al. . (2006). Non-invasive monitoring of renal oxygenation using BOLD-MRI: a reproducibility study. NMR Biomed. 19, 84–89. 10.1002/nbm.1004
    1. Skorecki K., Chertow G. M., Marsden P. A., Taal M. W., Yu A. S. L. (2016). Brenner and Rector's The Kidney, 10th Edn. Philadelphia, PA: Elsevier.
    1. Steeden J. A., Muthurangu V. (2015). Investigating the limitations of single breath-hold renal artery blood flow measurements using spiral phase contrast MR with R-R interval averaging. J. Magn. Reson. Imaging 41, 1143–1149. 10.1002/jmri.24638
    1. Suo S., Lin N., Wang H., Zhang L., Wang R., Zhang S., et al. . (2015). Intravoxel incoherent motion diffusion-weighted MR imaging of breast cancer at 3.0 Tesla: comparison of different curve-fitting methods. J. Magn. Reson. Imaging 42, 362–370. 10.1002/jmri.24799
    1. Tan H., Koktzoglou I., Prasad P. V. (2014). Renal perfusion imaging with two-dimensional navigator gated arterial spin labeling. Magn. Reson. Med. 71, 570–579. 10.1002/mrm.24692
    1. Thoeny H. C., De Keyzer F., Oyen R. H., Peeters R. R. (2005). Diffusion-weighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience. Radiology 235, 911–917. 10.1148/radiol.2353040554
    1. Thomson S. C., Blantz R. C. (2008). Glomerulotubular balance, tubuloglomerular feedback, and salt homeostasis. J. Am. Soc. Nephrol. 19, 2272–2275. 10.1681/ASN.2007121326
    1. Tumkur S. M., Vu A. T., Li L. P., Pierchala L., Prasad P. V. (2006a). Evaluation of intra-renal oxygenation during water diuresis: a time-resolved study using BOLD MRI. Kidney Int. 70, 139–143. 10.1038/sj.ki.5000347
    1. Tumkur S., Vu A., Li L., Prasad P. V. (2006b). Evaluation of intrarenal oxygenation at 3.0 T using 3-dimensional multiple gradient-recalled echo sequence. Invest. Radiol. 41, 181–184. 10.1097/01.rli.0000187166.43871.fb
    1. Tunnicliffe E. M., Banerjee R., Pavlides M., Neubauer S., Robson M. D. (2017). A model for hepatic fibrosis: the competing effects of cell loss and iron on shortened modified Look-Locker inversion recovery T1 (shMOLLI-T1) in the liver. J. Magn. Reson. Imaging 45, 450–462. 10.1002/jmri.25392
    1. van den Dool S. W., Wasser M. N., de Fijter J. W., Hoekstra J., van der Geest R. J. (2005). Functional renal volume: quantitative analysis at gadolinium-enhanced MR angiography–feasibility study in healthy potential kidney donors. Radiology 236, 189–195. 10.1148/radiol.2361021463
    1. van der Bel R., Coolen B. F., Nederveen A. J., Potters W. V., Verberne H. J., Vogt L., et al. . (2016). Magnetic resonance imaging-derived renal oxygenation and perfusion during continuous, steady-state angiotensin-II infusion in healthy humans. J. Am. Heart Assoc. 5:e003185. 10.1161/JAHA.115.003185
    1. Venkatachalam M. A., Griffin K. A., Lan R., Geng H., Saikumar P., Bidani A. K. (2010). Acute kidney injury: a springboard for progression in chronic kidney disease. Am. J. Physiol. Renal Physiol. 298, F1078–F1094. 10.1152/ajprenal.00017.2010
    1. Vivier P. H., Storey P., Chandarana H., Yamamoto A., Tantillo K., Khan U., et al. (2013). Renal blood oxygenation level-dependent imaging: contribution of R2 to R2* values. Invest. Radiol. 48, 501–508. 10.1097/RLI.0b013e3182823591
    1. Wang J., Zhang Y., Yang X., Wang X., Zhang J., Fang J., et al. . (2012). Hemodynamic effects of furosemide on renal perfusion as evaluated by ASL-MRI. Acad. Radiol. 19, 1194–1200. 10.1016/j.acra.2012.04.021
    1. Winter J. D., Estrada M., Cheng H. L. (2011). Normal tissue quantitative T1 and T2* MRI relaxation time responses to hypercapnic and hyperoxic gases. Acad. Radiol. 18, 1159–1167. 10.1016/j.acra.2011.04.016
    1. Wittsack H. J., Lanzman R. S., Mathys C., Janssen H., Modder U., Blondin D. (2010). Statistical evaluation of diffusion-weighted imaging of the human kidney. Magn. Reson. Med. 64, 616–622. 10.1002/mrm.22436
    1. Xin-Long P., Jing-Xia X., Jian-Yu L., Song W., Xin-Kui T. (2012). A preliminary study of blood-oxygen-level-dependent MRI in patients with chronic kidney disease. Magn. Reson. Imaging 30, 330–335. 10.1016/j.mri.2011.10.003
    1. Young I. R., Clarke G. J., Bailes D. R., Pennock J. M., Doyle F. H., Bydder G. M. (1981). Enhancement of relaxation rate with paramagnetic contrast agents in NMR imaging. J. Comput. Tomogr. 5, 543–547. 10.1016/0149-936X(81)90089-8
    1. Zhang J. L., Sigmund E. E., Chandarana H., Rusinek H., Chen Q., Vivier P. H., et al. . (2010). Variability of renal apparent diffusion coefficients: limitations of the monoexponential model for diffusion quantification. Radiology 254, 783–792. 10.1148/radiol.09090891

Source: PubMed

3
Suscribir