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      Renal blood oxygenation level-dependent magnetic resonance imaging to measure renal tissue oxygenation: a statement paper and systematic review

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          Abstract

          Tissue hypoxia plays a key role in the development and progression of many kidney diseases. Blood oxygenation level-dependent magnetic resonance imaging (BOLD-MRI) is the most promising imaging technique to monitor renal tissue oxygenation in humans. BOLD-MRI measures renal tissue deoxyhaemoglobin levels voxel by voxel. Increases in its outcome measure R2* (transverse relaxation rate expressed as per second) correspond to higher deoxyhaemoglobin concentrations and suggest lower oxygenation, whereas decreases in R2* indicate higher oxygenation. BOLD-MRI has been validated against micropuncture techniques in animals. Its reproducibility has been demonstrated in humans, provided that physiological and technical conditions are standardized. BOLD-MRI has shown that patients suffering from chronic kidney disease (CKD) or kidneys with severe renal artery stenosis have lower tissue oxygenation than controls. Additionally, CKD patients with the lowest cortical oxygenation have the worst renal outcome. Finally, BOLD-MRI has been used to assess the influence of drugs on renal tissue oxygenation, and may offer the possibility to identify drugs with nephroprotective or nephrotoxic effects at an early stage. Unfortunately, different methods are used to prepare patients, acquire MRI data and analyse the BOLD images. International efforts such as the European Cooperation in Science and Technology (COST) action ‘Magnetic Resonance Imaging Biomarkers for Chronic Kidney Disease’ (PARENCHIMA) are aiming to harmonize this process, to facilitate the introduction of this technique in clinical practice in the near future. This article represents an extensive overview of the studies performed in this field, summarizes the strengths and weaknesses of the technique, provides recommendations about patient preparation, image acquisition and analysis, and suggests clinical applications and future developments.

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          Determinants of kidney oxygen consumption and their relationship to tissue oxygen tension in diabetes and hypertension.

          The high renal oxygen (O(2) ) demand is associated primarily with tubular O(2) consumption (Qo(2) ) necessary for solute reabsorption. Increasing O(2) delivery relative to demand via increased blood flow results in augmented tubular electrolyte load following elevated glomerular filtration, which, in turn, increases metabolic demand. Consequently, elevated kidney metabolism results in decreased tissue oxygen tension. The metabolic efficiency for solute transport (Qo(2) /T(Na) ) varies not only between different nephron sites, but also under different conditions of fluid homeostasis and disease. Contributing mechanisms include the presence of different Na(+) transporters, different levels of oxidative stress and segmental tubular dysfunction. Sustained hyperglycaemia results in increased kidney Qo(2) , partly due to mitochondrial dysfunction and reduced electrolyte transport efficiency. This results in intrarenal tissue hypoxia because the increased Qo(2) is not matched by a similar increase in O(2) delivery. Hypertension leads to renal hypoxia, mediated by increased angiotensin receptor tonus and oxidative stress. Reduced uptake in the proximal tubule increases load to the thick ascending limb. There, the increased load is reabsorbed, but at greater O(2) cost. The combination of hypertension, angiotensin II and oxidative stress initiates events leading to renal damage and reduced function. Tissue hypoxia is now recognized as a unifying pathway to chronic kidney disease. We have gained good knowledge about major changes in O(2) metabolism occurring in diabetic and hypertensive kidneys. However, further efforts are needed to elucidate how these alterations can be prevented or reversed before translation into clinical practice. © 2012 The Authors Clinical and Experimental Pharmacology and Physiology © 2012 Wiley Publishing Asia Pty Ltd.
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            Autologous Mesenchymal Stem Cells Increase Cortical Perfusion in Renovascular Disease.

            Atherosclerotic renovascular disease (RVD) reduces renal blood flow (RBF) and GFR and accelerates poststenotic kidney (STK) tissue injury. Preclinical studies indicate that mesenchymal stem cells (MSCs) can stimulate angiogenesis and modify immune function in experimental RVD. We assessed the safety and efficacy of adding intra-arterial autologous adipose-derived MSCs into STK to standardized medical treatment in human subjects without revascularization. The intervention group (n=14) received a single infusion of MSC (1.0 × 10(5) or 2.5 × 10(5) cells/kg; n=7 each) plus standardized medical treatment; the medical treatment only group (n=14) included subjects matched for age, kidney function, and stenosis severity. We measured cortical and medullary volumes, perfusion, and RBF using multidetector computed tomography. We assessed tissue oxygenation by blood oxygen level-dependent MRI and GFR by iothalamate clearance. MSC infusions were well tolerated. Three months after infusion, cortical perfusion and RBF rose in the STK (151.8-185.5 ml/min, P=0.01); contralateral kidney RBF increased (212.7-271.8 ml/min, P=0.01); and STK renal hypoxia (percentage of the whole kidney with R2*>30/s) decreased (12.1% [interquartile range, 3.3%-17.8%] to 6.8% [interquartile range, 1.8%-12.9%], P=0.04). No changes in RBF occurred in medical treatment only subjects. Single-kidney GFR remained stable after MSC but fell in the medical treatment only group (-3% versus -24%, P=0.04). This first-in-man dose-escalation study provides evidence of safety of intra-arterial infusion of autologous MSCs in patients with RVD. MSC infusion without main renal artery revascularization associated with increased renal tissue oxygenation and cortical blood flow.
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              Reduced cortical oxygenation predicts a progressive decline of renal function in patients with chronic kidney disease

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                Author and article information

                Journal
                Nephrol Dial Transplant
                Nephrol. Dial. Transplant
                ndt
                Nephrology Dialysis Transplantation
                Oxford University Press
                0931-0509
                1460-2385
                September 2018
                23 August 2018
                23 August 2018
                : 33
                : Suppl 2 , Magnetic Resonance Imaging Biomarkers in Renal Disease
                : ii22-ii28
                Affiliations
                [1 ]Service of Nephrology and Hypertension, Department of Medicine, University Hospital of Lausanne (CHUV), Lausanne, Switzerland
                [2 ]Department of Radiology, Cambridge University Hospitals NHS Foundation Trust, Addenbrooke’s Hospital, Cambridge, UK
                [3 ]Department of Surgical Sciences, Section of Radiology, Uppsala University, Uppsala, Sweden
                [4 ]Department of Nephrology and Hypertension, Universitair Ziekenhuis Brussel (VUB), Brussels, Belgium
                [5 ]Division of Nephrology and Hypertension, Mayo Clinic, Rochester, MN, USA
                [6 ]Department of Internal Medicine, Division of Nephrology, Academic Medical Center at the University of Amsterdam, Amsterdam, The Netherlands
                [7 ]Medical Imaging Unit, Bioengineering Department, IRCCS Istituto di Ricerche Farmacologiche Mario Negri, Bergamo, Italy
                [8 ]Department of Radiology, NorthShore University HealthSystem, Evanston, IL, USA
                Author notes
                Correspondence and offprint requests to: Menno Pruijm; E-mail: menno.pruijm@ 123456chuv.ch ; Twitter handle: @renalMRI
                Article
                gfy243
                10.1093/ndt/gfy243
                6106642
                30137579
                a82b5140-2552-43c0-a724-45a9447e7099
                © The Author(s) 2018. Published by Oxford University Press on behalf of ERA-EDTA.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 25 April 2018
                : 27 June 2018
                Page count
                Pages: 7
                Funding
                Funded by: Swiss National Science Foundation 10.13039/501100001711
                Award ID: FN 320030-169191
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: R01DK093793
                Categories
                Reviews

                Nephrology
                bold-mri,chronic kidney disease,functional mri,kidney,renal artery stenosis
                Nephrology
                bold-mri, chronic kidney disease, functional mri, kidney, renal artery stenosis

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