Consensus-based technical recommendations for clinical translation of renal ASL MRI
Tóm tắt
This study aimed at developing technical recommendations for the acquisition, processing and analysis of renal ASL data in the human kidney at 1.5 T and 3 T field strengths that can promote standardization of renal perfusion measurements and facilitate the comparability of results across scanners and in multi-centre clinical studies.
An international panel of 23 renal ASL experts followed a modified Delphi process, including on-line surveys and two in-person meetings, to formulate a series of consensus statements regarding patient preparation, hardware, acquisition protocol, analysis steps and data reporting.
Fifty-nine statements achieved consensus, while agreement could not be reached on two statements related to patient preparation. As a default protocol, the panel recommends pseudo-continuous (PCASL) or flow-sensitive alternating inversion recovery (FAIR) labelling with a single-slice spin-echo EPI readout with background suppression and a simple but robust quantification model.
This approach is considered robust and reproducible and can provide renal perfusion images of adequate quality and SNR for most applications. If extended kidney coverage is desirable, a 2D multislice readout is recommended. These recommendations are based on current available evidence and expert opinion. Nonetheless they are expected to be updated as more data become available, since the renal ASL literature is rapidly expanding.
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Tài liệu tham khảo
Evans RG, Gardiner BS, Smith DW, O’Connor PM (2008) Methods for studying the physiology of kidney oxygenation. Clin Exp Pharmacol Physiol 35:1405–1412
Singh P, Ricksten S-E, Bragadottir G, Redfors B, Nordquist L (2013) Renal oxygenation and haemodynamics in acute kidney injury and chronic kidney disease. Clin Exp Pharmacol Physiol 40:138–147
Ow CPC, Ngo JP, Ullah MM, Hilliard LM, Evans RG (2018) Renal hypoxia in kidney disease: cause or consequence? Acta Physiol 222:e12999
Williams DS, Detre JA, Leigh JS, Koretsky AP (1992) Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci 89:212–216
Roberts DA, Detre JA, Bolinger L, Insko EK, Lenkinski RE, Pentecost MJ, Leigh JS (1995) Renal perfusion in humans: MR imaging with spin tagging of arterial water. Radiology 196:281–286
Schieda N, Blaichman JI, Costa AF, Glikstein R, Hurrell C, James M, Jabehdar Maralani P, Shabana W, Tang A, Tsampalieros A, van der Pol C, Hiremath S (2018) Gadolinium-based contrast agents in kidney disease: comprehensive Review and Clinical Practice Guideline Issued by the Canadian Association of Radiologists. Can Assoc Radiol J 69:136–150
Odudu A, Nery F, Harteveld AA, Evans RG, Pendse D, Buchanan CE, Francis ST, Fernández-Seara MA (2018) Arterial spin labelling MRI to measure renal perfusion: a systematic review and statement paper. Nephrol Dial Transplant 33:ii15–ii21.
Nery F, Gordon I, Thomas D (2018) Non-invasive renal perfusion imaging using arterial spin labeling MRI: challenges and opportunities. Diagnostics 8:2
Bones IK, Harteveld AA, Franklin SL, van Osch MJP, Hendrikse J, Moonen CTW, Bos C, van Stralen M (2019) Enabling free-breathing background suppressed renal pCASL using fat imaging and retrospective motion correction. Magn Reson Med. https://doi.org/10.1002/mrm.27723
Buchanan CE, Cox EF, Francis ST (2018) Evaluation of 2D imaging schemes for pulsed arterial spin labeling of the human kidney cortex. Diagnostics 8:43
Eckerbom P, Hansell P, Cox E, Buchanan C, Weis J, Palm F, Francis S, Liss P (2019) Multiparametric assessment of renal physiology in healthy volunteers using noninvasive magnetic resonance imaging. Am J Physiol Physiol 316:F693–F702
Greer JS, Wang X, Wang Y, Pinho MC, Maldjian JA, Pedrosa I, Madhuranthakam AJ (2019) Robust pCASL perfusion imaging using a 3D Cartesian acquisition with spiral profile reordering (CASPR). Magn Reson Med. https://doi.org/10.1002/mrm.27862
BT Haddock ST Francis HBW Larsson UB Andersen 2018 Assessment of perfusion and oxygenation of the human renal cortex and medulla by quantitative MRI during Handgrip Exercise J Am Soc Nephrol
Haddock B, Larsson HBW, Francis S, Andersen UB (2019) Human renal response to furosemide: Simultaneous oxygenation and perfusion measurements in cortex and medulla. Acta Physiol 0:e13292.
Hellms S, Gueler F, Gutberlet M, Schebb NH, Rund K, Kielstein JT, VoChieu V, Rauhut S, Greite R, Martirosian P, Haller H, Wacker F, Derlin K (2019) Single‐dose diclofenac in healthy volunteers can cause decrease in renal perfusion measured by functional magnetic resonance imaging. J Pharm Pharmacol 0:jphp.13105.
Nery F, De Vita E, Clark CA, Gordon I, Thomas DL (2019) Robust kidney perfusion mapping in pediatric chronic kidney disease using single-shot 3D-GRASE ASL with optimized retrospective motion correction. Magn Reson Med 81:2972–2984
Prasad PV, Li L-P, Thacker JM, Li W, Hack B, Kohn O, Sprague SM (2019) Cortical perfusion and tubular function as evaluated by magnetic resonance imaging correlates with annual loss in renal function in moderate chronic kidney disease. Am J Nephrol 49:114–124
Shirvani S, Tokarczuk P, Statton B, Quinlan M, Berry A, Tomlinson J, Weale P, Kühn B, O’Regan DP (2019) Motion-corrected multiparametric renal arterial spin labelling at 3 T: reproducibility and effect of vasodilator challenge. Eur Radiol 29:232–240
Taso M, Guidon A, Alsop DC (2019) Influence of background suppression and retrospective realignment on free-breathing renal perfusion measurement using pseudo-continuous ASL. Magn Reson Med 81:2439–2449
Taso M, Zhao L, Guidon A, Litwiller DV, Alsop DC (2019) Volumetric abdominal perfusion measurement using a pseudo-randomly sampled 3D fast-spin-echo (FSE) arterial spin labeling (ASL) sequence and compressed sensing reconstruction. Magn Reson Med 82:680–692
Dai W, Garcia DM, de Bazelaire C, Alsop DC (2008) Continuous flow driven inversion for arterial spin labelling using pulsed radiofrequency and gradient fields. Magn Reson Med 60:1488–1497
Wu W-C, Fernández-Seara M, Detre JA, Wehrli FW, Wang J (2007) A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn Reson Med 58:1020–1027
Kwong KK, Chesler DA, Weisskoff RM, Donahue KM, Davis TL, Ostergaard L, Campbell TA, Rosen BR (1995) Mr perfusion studies with t1-weighted echo planar imaging. Magn Reson Med 34:878–887
Kim SG, Tsekos NV (1997) Perfusion imaging by a flow-sensitive alternating inversion recovery (FAIR) technique: application to functional brain imaging. Magn Reson Med 37:425–435
Wong EC, Buxton RB, Frank LR (1998) Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn Reson Med 39:702–708
Luh WM, Wong EC, Bandettini PA, Hyde JS (1999) QUIPSS II with thin-slice TI1 periodic saturation: a method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magn Reson Med 41:1246–1254
Helmer O (1967) Analysis of the future: the delphi method. Rand Corp.
Hsu C-C, Sandford BA (2007) The Delphi Technique: Making Sense Of Consensus. Pract Assessment, Res Eval 12:1–8
Yousuf MI (2007) Using experts’ opinions through delphi technique. Pract Assessment, Res Eval. https://doi.org/10.1016/S0169-2070(99)00018-7
Mendichovszky I, Pullens P, Dekkers I, Nery F, Bane O, Pohlmann A, de Boer A, Ljimani A, Odudu A, Buchanan C, Sharma K, Laustsen C, Harteveld A, Golay X, Pedrosa I, Alsop D, Fain S, Caroli A, Prasad P, Francis S, Sigmund E, Fernández-Seara M, Sourbron S (2019) Technical recommendations for clinical translation of renal MRI: a consensus project of the Cooperation in Science and Technology Action PARENCHIMA. Magn Reson Mater Phy. https://doi.org/10.1007/s10334-019-00784-w
Taylor SA, Avni F, Cronin CG, Hoeffel C, Kim SH, Laghi A, Napolitano M, Petit P, Rimola J, Tolan DJ, Torkzad MR, Zappa M, Bhatnagar G, Puylaert CAJ, Stoker J (2017) The first joint ESGAR/ ESPR consensus statement on the technical performance of cross-sectional small bowel and colonic imaging. Eur Radiol 27:2570–2582
Muller BG, Van Den Bos W, Brausi M, Cornud F, Gontero P, Kirkham A, Pinto PA, Polascik TJ, Rastinehad AR, De Reijke TM, De La Rosette JJ, Ukimura O, Villers A, Walz J, Wijkstra H, Marberger M (2014) Role of multiparametric magnetic resonance imaging (MRI) in focal therapy for prostate cancer: a Delphi consensus project. BJU Int 114:698–707
Katragadda C, Finnane A, Soyer HP, Marghoob AA, Halpern A, Malvehy J, Kittler H, Hofmann-Wellenhof R, Da Silva D, Abraham I, Curiel-Lewandrowski C (2017) Technique standards for skin lesion imaging a delphi consensus statement. JAMA Dermatology 153:207–213
Armstrong LE (2007) Assessing hydration status: the elusive gold standard. J Am Coll Nutr 26:575S–584S
Wabel P, Chamney P, Moissl U, Jirka T (2009) Importance of whole-body bioimpedance spectroscopy for the management of fluid balance. Blood Purif. pp 75–80
Wang J, Zhang Y, Yang X, Wang X, Zhang J, Fang J, Jiang X (2012) Hemodynamic effects of furosemide on renal perfusion as evaluated by ASL-MRI. Acad Radiol 19:1194–1200
He X, Aghayev A, Gumus S, Ty Bae K (2014) Estimation of single-kidney glomerular filtration rate without exogenous contrast agent. Magn Reson Med 71:257–266
Boss A, Martirosian P, Graf H, Claussen CD, Schlemmer HP, Schick F (2005) High resolution MR perfusion imaging of the kidneys at 3 Tesla without administration of contrast media. Rofo 177:1625–1630
Gillis KA, McComb C, Foster JE, Taylor AHM, Patel RK, Morris STW, Jardine AG, Schneider MP, Roditi GH, Delles C, Mark PB (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
Heusch P, Wittsack HJ, Blondin D, Ljimani A, Nguyen-Quang M, Martirosian P, Zenginli H, Bilk P, Kröpil P, Heusner TA, Antoch G, Lanzman RS (2014) Functional evaluation of transplanted kidneys using arterial spin labeling MRI. J Magn Reson Imaging 40:84–89
Cutajar M, Thomas DL, Banks T, Clark CA, Golay X, Gordon I (2012) Repeatability of renal arterial spin labelling MRI in healthy subjects. Magn Reson Mater Phy 25:145–153
Cox EF, Buchanan CE, Bradley CR, Prestwich B, Mahmoud H, Taal M, Selby NM, Francis ST (2017) Multiparametric renal magnetic resonance imaging: Validation, interventions, and alterations in chronic kidney disease. Front Physiol 8:696
Shimizu K, Kosaka N, Fujiwara Y, Matsuda T, Yamamoto T, Tsuchida T, Tsuchiyama K, Oyama N, Kimura H (2017) Arterial transit time-corrected renal blood flow measurement with pulsed continuous arterial spin labeling MR imaging. Magn Reson Med Sci 16:38–44
Ordidge RJ, Wylezinska M, Hugg JW, Butterworth E, Franconi F (1996) Frequency offset corrected inversion (FOCI) pulses for use in localized spectroscopy. Magn Reson Med 36:562–566
Wang X, Greer JS, Dimitrov IE, Pezeshk P, Chhabra A, Madhuranthakam AJ (2018) Frequency offset corrected inversion pulse for B0 and B1 insensitive fat suppression at 3T: application to MR neurography of brachial plexus. J Magn Reson Imaging 48:1104–1111
Tan H, Koktzoglou I, Prasad PV (2014) Renal perfusion imaging with two-dimensional navigator gated arterial spin labeling. Magn Reson Med 71:570–579
Cai Y, Li Z, Zuo P, Pfeuffer J, Li Y, Liu F, Liu R (2017) Diagnostic value of renal perfusion in patients with chronic kidney disease using 3D arterial spin labeling. J Magn Reson Imaging 46:589–594
Wong EC, Buxton RB, Frank LR (1998) A theoretical and experimental comparison of continuous and pulsed arterial spin labeling techniques for quantitative perfusion imaging. Magn Reson Med 40:348–355
Zhao L, Vidorreta M, Soman S, Detre JA, Alsop DC (2017) Improving the robustness of pseudo-continuous arterial spin labeling to off-resonance and pulsatile flow velocity. Magn Reson Med 78:1342–1351
Greer JS, Wang Y, Pedrosa I, Madhuranthakam AJ (2019) Pseudo-continuous arterial spin labeled renal perfusion imaging at 3T with improved robustness to off-resonance. Proc. ISMRM 27th Annu. Meet. Exhib. Montr. QC, Canada. p 4959
Echeverria-Chasco R, Vidorreta M, Aramendía-Vidaurreta V, Bastarrika G, Fernández-Seara MA (2019) Optimization of pseudo continuous arterial spin labeling for renal ASL. Proc. ISMRM 27th Annu. Meet. Exhib. Montr. QC, Canada. p 4954
Alsop DC, Detre JA, Golay X, Günther M, Hendrikse J, Hernandez-Garcia L, Lu H, Macintosh BJ, Parkes LM, Smits M, Van Osch MJP, Wang DJJ, Wong EC, Zaharchuk G (2015) Recommended implementation of arterial spin-labeled Perfusion MRI for clinical applications: a consensus of the ISMRM perfusion Study group and the European consortium for ASL in dementia. Magn Reson Med 73:102–116
Robson PM, Madhuranthakam AJ, Dai W, Pedrosa I, Rofsky NM, Alsop DC (2009) Strategies for reducing respiratory motion artifacts in renal perfusion imaging with arterial spin labeling. Magn Reson Med 61:1374–1387
Wu W-C, Su M-Y, Chang C-C, Tseng W-YI, Liu K-L (2011) Renal perfusion 3-T MR imaging: a comparative study of arterial spin labeling and dynamic contrast-enhanced techniques. Radiology 261:845–853
Robson PM, Madhuranthakam AJ, Smith MP, Sun MRM, Dai W, Rofsky NM, Pedrosa I, Alsop DC (2016) Volumetric arterial spin-labeled perfusion imaging of the kidneys with a three-dimensional fast spin echo acquisition. Acad Radiol 23:144–154
Mora-Gutiérrez JM, Garcia-Fernandez N, Slon Roblero MF, Páramo JA, Escalada FJ, Wang DJ, Benito A, Fernández-Seara MA (2017) Arterial spin labeling MRI is able to detect early hemodynamic changes in diabetic nephropathy. J Magn Reson Imaging 1–8.
Song H, Ruan D, Liu W, Stenger VA, Pohmann R, Fernández-Seara MA, Nair T, Jung S, Luo J, Motai Y, Ma J, Hazle JD, Gach HM (2017) Respiratory motion prediction and prospective correction for free-breathing arterial spin-labeled perfusion MRI of the kidneys. Med Phys 44:962–973
Rapacchi S, Smith RX, Wang Y, Yan L, Sigalov V, Krasileva KE, Karpouzas G, Plotnik A, Sayre J, Hernandez E, Verma A, Burkly L, Wisniacki N, Torrington J, He X, Hu P, Chiao PC, Wang DJJ (2015) Towards the identification of multi-parametric quantitative MRI biomarkers in lupus nephritis. Magn Reson Imaging 33:1066–1074
Aslan A, Van Den Heuvel MC, Stegeman CA, Popa ER, Leliveld AM, Molema G, Zijlstra JG, Moser J, Van Meurs M (2018) Kidney histopathology in lethal human sepsis. Crit Care. https://doi.org/10.1186/s13054-018-2287-3
Martirosian P, Klose U, Mader I, Schick F (2004) FAIR true-FISP perfusion imaging of the kidneys. Magn Reson Med 51:353–361
Gardener AG, Francis ST (2010) Multislice perfusion of the kidneys using parallel imaging: image acquisition and analysis strategies. Magn Reson Med 63:1627–1636
de Bazelaire C, Rofsky NM, Duhamel G, Michaelson MD, George D, Alsop DC (2005) Arterial spin labeling blood flow magnetic resonance imaging for the characterization of metastatic renal cell carcinoma. Acad Radiol 12:347–357
Golay X, Petersen ET, Hui F (2005) Pulsed star labeling of arterial regions (PULSAR): a robust regional perfusion technique for high field imaging. Magn Reson Med 53:15–21
Günther M (2006) Efficient visualization of vascular territories in the human brain by cycled arterial spin labeling MRI. Magn Reson Med 56:671–675
Ye FQ, Berman KF, Ellmore T, Esposito G, Van Horn JD, Yang Y, Duyn J, Smith AM, Frank JA, Weinberger DR, McLaughlin AC (2000) H2–15-O PET validation of steady-state arterial spin tagging cerebral blood flow measurements in humans. Magn Reson Med 44:450–456
Maleki N, Dai W, Alsop DC (2012) Optimization of background suppression for arterial spin labeling perfusion imaging. Magn Reson Mater Phy 25:127–133
Garcia DM, Duhamel G, Alsop DC (2005) Efficiency of inversion pulses for background suppressed arterial spin labeling. Magn Reson Med 54:366–372
Chavhan GB, Babyn PS, Vasanawala SS (2013) Abdominal MR imaging in children: motion compensation, sequence optimization, and protocol organization. Radiographics 33:703–719
Dong J, Yang L, Su T, Yang X, Chen B, Zhang J, Wang X, Jiang X (2013) Quantitative assessment of acute kidney injury by noninvasive arterial spin labeling perfusion MRI: a pilot study. Sci China Life Sci 56:745–750
Conlin CC, Oesingmann N, Bolster B, Huang Y, Lee VS, Zhang JL (2017) Renal plasma flow (RPF) measured with multiple-inversion-time arterial spin labeling (ASL) and tracer kinetic analysis: Validation against a dynamic contrast-enhancement method. Magn Reson Imaging 37:51–55
Niles DJ, Artz NS, Djamali A, Sadowski EA, Grist TM, Fain SB (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
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
Fenchel M, Martirosian P, Langanke J, Giersch J, Miller S, Stauder NI, Kramer U, Claussen CD, Schick F (2006) Perfusion MR imaging with FAIR true FISP spin labeling in patients with and without renal artery stenosis: initial experience. Radiology 238:1013–1021
Artz NS, Sadowski EA, Wentland AL, Grist TM, Seo S, Djamali A, Fain SB (2011) Arterial spin labeling MRI for assessment of perfusion in native and transplanted kidneys. Magn Reson Imaging 29:74–82
Song R, Tipirneni A, Johnson P, Loeffler RB, Hillenbrand CM (2011) Evaluation of respiratory liver and kidney movements for MRI navigator gating. J Magn Reson Imaging 33:143–148
Siva S, Pham D, Gill S, Bressel M, Dang K, Devereux T, Kron T, Foroudi F (2013) An analysis of respiratory induced kidney motion on four-dimensional computed tomography and its implications for stereotactic kidney radiotherapy. Radiat Oncol 8:248
Mutsaerts HJMM, Petr J, Thomas DL, Vita E de, Cash DM, Osch MJP van, Golay X, Groot PFC, Ourselin S, Swieten J van, Laforce R, Tagliavini F, Borroni B, Galimberti D, Rowe JB, Graff C, Pizzini FB, Finger E, Sorbi S, Castelo Branco M, Rohrer JD, Masellis M, MacIntosh BJ (2017) Comparison of arterial spin labeling registration strategies in the multi-center GENetic frontotemporal dementia initiative (GENFI). J Magn Reson Imaging 1–10.
Alsop DC, Detre JA (1996) Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. J Cereb Blood Flow Metab 16:1236–1249
Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR (1998) A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 40:383–396
Yuasa Y, Kundel HL (1985) Magnetic resonance imaging following unilateral occlusion of the renal circulation in rabbits. Radiology 154:151–156
Kundel HL, Schlakman B, Joseph PM, Fishman JE, Summers R (1986) Water content and NMR relaxation time gradients in the rabbit kidney. Invest Radiol 21:12–17
Pedersen M, Vajda Z, Stødkilde-Jørgensen H, Nielsen S, Frøkiær J (2007) Furosemide increases water content in renal tissue. Am J Physiol Ren Physiol. https://doi.org/10.1152/ajprenal.00060.2006
Liu HS, Jawad AF, Laney N, Hartung EA, Furth SL, Detre JA (2019) Effect of blood T1 estimation strategy on arterial spin labeled cerebral blood flow quantification in children and young adults with kidney disease. J Neuroradiol 46:29–35
Song R, Loeffler RB, Hillenbrand CM (2010) Improved renal perfusion measurement with a dual navigator-gated Q2TIPS fair technique. Magn Reson Med 64:1352–1359
Karger N, Biederer J, Lusse S, Grimm J, Steffens J-C, Heller M, Gluer C-C (2000) Quantitation of renal perfusion using arterial spin labeling with FAIR-UFLARE. Magn Reson Imaging 18:641–647
Noda Y, Ito K, Kanki A, Tamada T, Yamamoto A, Kazuya Y, Higaki A (2015) Measurement of renal cortical thickness using noncontrast-enhanced steady-state free precession MRI with spatially selective inversion recovery pulse: Association with renal function. J Magn Reson Imaging 41:1615–1621
Takata T, Koda M, Sugihara T, Sugihara S, Okamoto T, Miyoshi K, Hodotsuka M, Fujise Y, Matono T, Okano J, Hosho K, Iyama T, Fukui T, Fukuda S, Munemura C, Isomoto H (2016) Left renal cortical thickness measured by ultrasound can predict early progression of chronic kidney disease. Nephron 132:25–32
Korkmaz M, Aras B, Güneyli S, Yılmaz M (2018) Clinical significance of renal cortical thickness in patients with chronic kidney disease. Ultrasonography 37:50–54
Otsuka T, Kaneko Y, Sato Y, Kaseda R, Aoyagi R, Yamamoto S, Goto S, Narita I (2018) Kidney morphological parameters measured using noncontrast-enhanced steady-state free precession MRI with spatially selective inversion recovery pulse correlate with eGFR in patients with advanced CKD. Clin Exp Nephrol 22:45–54
Wang JH, Skeans MA, Israni AK (2016) Current status of kidney transplant outcomes: dying to survive. Adv Chronic Kidney Dis 23:281–286
Sadowski EA, Djamali A, Wentland AL, Muehrer R, Becker BN, Grist TM, Fain SB (2010) Blood oxygen level-dependent and perfusion magnetic resonance imaging: detecting differences in oxygen bioavailability and blood flow in transplanted kidneys. Magn Reson Imaging 28:56–64
Moore JE, Maier SE, Ku DN, Boesiger P (1994) Hemodynamics in the abdominal aorta: a comparison of in vitro and in vivo measurements. J Appl Physiol 76:1520–1527
Bradley CR, Buchanan CE, Cox EF, Francis ST (2018) Assessment of optimal technique for measurement of medullary perfusion. Proc. ISMRM 26th Annu. Meet. Exhib. Paris, Fr. 4600
Herscovitch P, Raichle ME (1985) What is the correct value for the brain-blood partition coefficient for water? J Cereb Blood Flow Metab 5:65–69