Skip to main content
Erschienen in: Magnetic Resonance Materials in Physics, Biology and Medicine 3/2018

01.06.2018 | Research Article

Assessing renal changes after remote ischemic preconditioning (RIPC) of the upper extremity using BOLD imaging at 3T

verfasst von: Florian Siedek, Thorsten Persigehl, Roman-Ulrich Mueller, Volker Burst, Thomas Benzing, David Maintz, Stefan Haneder

Erschienen in: Magnetic Resonance Materials in Physics, Biology and Medicine | Ausgabe 3/2018

Einloggen, um Zugang zu erhalten

Abstract

Objective

Acute kidney injury (AKI) is an important risk factor for a number of adverse outcomes including end-stage renal disease and cardiovascular morbidity and mortality. Whilst many clinical situations that can induce AKI are known—e.g. drug toxicity, contrast agent exposure or ischemia during surgery—targeted preventive or therapeutic measures are still lacking. As to renoprotective strategies, remote ischemic preconditioning (RIPC) is one of the most promising novel approaches and has been examined by a number of clinical trials. The aim of this study was to use blood oxygenation level-dependent (BOLD) MRI as a surrogate parameter to assess the effect of RIPC in healthy volunteers.

Materials and methods

In this IRB-approved, prospective study, 40 healthy volunteers were stratified with 20 undergoing an RIPC procedure (i.e. RIPC group) with a transient ischemia of the right arm, and 20 undergoing a sham procedure. Before and after the procedure, both kidneys of all participants were scanned using a 12-echo mGRE sequence for functional BOLD imaging at 3T. For each volunteer, 180 ROIs were placed in the cortex and the medulla of the kidneys. Ultimately, R2* values, which have an inverse correlation with the oxygenation level of tissue, were averaged for the RIPC and control groups.

Results

Following intervention, mean R2* values significantly decreased in the RIPC group in both the cortex (18.6 ± 2.3 vs. 17.5 ± 1.7 Hz; p = 0.0047) and medulla (34 ± 5.2 vs. 32.2 ± 4.2 Hz; p = 0.0001). However, no significant differences were observed in the control group.

Conclusion

RIPC can be non-invasively assessed in healthy volunteers using BOLD MRI at 3T, demonstrating a higher oxygen content in kidney tissue. This study presents a first-in-man trial establishing a quantifiable readout of RIPC and its effects on kidney physiology. BOLD measurements may advance clinical trials in further evaluating RIPC for future clinical care.
Literatur
1.
Zurück zum Zitat McCullough PA, Adam A, Becker CR, Davidson C, Lameire N, Stacul F, Tumlin J, CIN Consensus Working Panel (2006) Epidemiology and prognostic implications of contrast-induced nephropathy. Am J Cardiol 98:5K–13KCrossRefPubMed McCullough PA, Adam A, Becker CR, Davidson C, Lameire N, Stacul F, Tumlin J, CIN Consensus Working Panel (2006) Epidemiology and prognostic implications of contrast-induced nephropathy. Am J Cardiol 98:5K–13KCrossRefPubMed
2.
Zurück zum Zitat Persson PB, Tepel M (2006) Contrast medium-induced nephropathy: the pathophysiology. Kidney Int Suppl 100:S8–10CrossRef Persson PB, Tepel M (2006) Contrast medium-induced nephropathy: the pathophysiology. Kidney Int Suppl 100:S8–10CrossRef
3.
Zurück zum Zitat Liss P, Nygren A, Olsson U, Ulfendahl HR, Erikson U (1996) Effects of contrast media and mannitol on renal medullary blood flow and red cell aggregation in the rat kidney. Kidney Int 49:1268–1275CrossRefPubMed Liss P, Nygren A, Olsson U, Ulfendahl HR, Erikson U (1996) Effects of contrast media and mannitol on renal medullary blood flow and red cell aggregation in the rat kidney. Kidney Int 49:1268–1275CrossRefPubMed
4.
Zurück zum Zitat Subramaniam RM, Suarez-Cuervo C, Wilson RF, Turban S, Zhang A, Sherrod C, Aboagye J, Eng J, Choi MJ, Hutfless S, Bass EB (2016) Effectiveness of prevention strategies for contrast-induced nephropathy: a systematic review and meta-analysis. Ann Intern Med 164:406–416CrossRefPubMed Subramaniam RM, Suarez-Cuervo C, Wilson RF, Turban S, Zhang A, Sherrod C, Aboagye J, Eng J, Choi MJ, Hutfless S, Bass EB (2016) Effectiveness of prevention strategies for contrast-induced nephropathy: a systematic review and meta-analysis. Ann Intern Med 164:406–416CrossRefPubMed
5.
Zurück zum Zitat Davenport MS, Cohan RH, Ellis JH (2015) Contrast media controversies in 2015: imaging patients with renal impairment or risk of contrast reaction. Am J Roentgenol 204:1174–1181CrossRef Davenport MS, Cohan RH, Ellis JH (2015) Contrast media controversies in 2015: imaging patients with renal impairment or risk of contrast reaction. Am J Roentgenol 204:1174–1181CrossRef
6.
Zurück zum Zitat Mitchell JR, Verweij M, Brand K, van de Ven M, Goemaere N, van den Engel S, Chu T, Forrer F, Müller C, de Jong M, van IJcken W, IJzermans JN, Hoeijmakers JH, de Bruin RW (2010) Short-term dietary restriction and fasting precondition against ischemia reperfusion injury in mice. Aging Cell 9:40–53CrossRefPubMed Mitchell JR, Verweij M, Brand K, van de Ven M, Goemaere N, van den Engel S, Chu T, Forrer F, Müller C, de Jong M, van IJcken W, IJzermans JN, Hoeijmakers JH, de Bruin RW (2010) Short-term dietary restriction and fasting precondition against ischemia reperfusion injury in mice. Aging Cell 9:40–53CrossRefPubMed
7.
Zurück zum Zitat Cochrane J, Williams BT, Banerjee A, Harken AH, Burke TJ, Cairns CB, Shapiro JI (1999) Ischemic preconditioning attenuates functional, metabolic, and morphologic injury from ischemic acute renal failure in the rat. Ren Fail 21:135–145CrossRefPubMed Cochrane J, Williams BT, Banerjee A, Harken AH, Burke TJ, Cairns CB, Shapiro JI (1999) Ischemic preconditioning attenuates functional, metabolic, and morphologic injury from ischemic acute renal failure in the rat. Ren Fail 21:135–145CrossRefPubMed
9.
Zurück zum Zitat Er F, Nia AM, Dopp H, Hellmich M, Dahlem KM, Caglayan E, Kubacki T, Benzing T, Erdmann E, Burst V, Gassanov N (2012) Ischemic preconditioning for prevention of contrast medium-induced nephropathy: randomized pilot RenPro trial (renal protection trial). Circulation 126:296–303CrossRefPubMed Er F, Nia AM, Dopp H, Hellmich M, Dahlem KM, Caglayan E, Kubacki T, Benzing T, Erdmann E, Burst V, Gassanov N (2012) Ischemic preconditioning for prevention of contrast medium-induced nephropathy: randomized pilot RenPro trial (renal protection trial). Circulation 126:296–303CrossRefPubMed
10.
Zurück zum Zitat Meybohm P, Bein B, Brosteanu O, Cremer J, Gruenewald M, Stoppe C, Coburn M, Schaelte G, Böning A, Niemann B, Roesner J, Kletzin F, Strouhal U, Reyher C, Laufenberg-Feldmann R, Ferner M, Brandes IF, Bauer M, Stehr SN, Kortgen A, Wittmann M, Baumgarten G, Meyer-Treschan T, Kienbaum P, Heringlake M, Schön J, Sander M, Treskatsch S, Smul T, Wolwender E, Schilling T, Fuernau G, Hasenclever D, Zacharowski K, RIPHeart Study Collaborators (2015) A multicenter trial of remote ischemic preconditioning for heart surgery. N Engl J Med 373:1397–1407CrossRefPubMed Meybohm P, Bein B, Brosteanu O, Cremer J, Gruenewald M, Stoppe C, Coburn M, Schaelte G, Böning A, Niemann B, Roesner J, Kletzin F, Strouhal U, Reyher C, Laufenberg-Feldmann R, Ferner M, Brandes IF, Bauer M, Stehr SN, Kortgen A, Wittmann M, Baumgarten G, Meyer-Treschan T, Kienbaum P, Heringlake M, Schön J, Sander M, Treskatsch S, Smul T, Wolwender E, Schilling T, Fuernau G, Hasenclever D, Zacharowski K, RIPHeart Study Collaborators (2015) A multicenter trial of remote ischemic preconditioning for heart surgery. N Engl J Med 373:1397–1407CrossRefPubMed
11.
Zurück zum Zitat Zarbock A, Kellum JA, Van Aken H, Schmidt C, Küllmar M, Rosenberger P, Martens S, Görlich D, Meersch M (2017) Long-term effects of remote ischemic preconditioning on kidney function in high-risk cardiac surgery patients: follow-up results from the renal RIP trial. Anesthesiology 126:787–798CrossRefPubMed Zarbock A, Kellum JA, Van Aken H, Schmidt C, Küllmar M, Rosenberger P, Martens S, Görlich D, Meersch M (2017) Long-term effects of remote ischemic preconditioning on kidney function in high-risk cardiac surgery patients: follow-up results from the renal RIP trial. Anesthesiology 126:787–798CrossRefPubMed
12.
Zurück zum Zitat Hausenloy DJ, Candilio L, Evans R, Ariti C, Jenkins DP, Kolvekar S, Knight R, Kunst G, Laing C, Nicholas JM, Pepper J, Robertson S, Xenou M, Clayton T, Yellon DM (2016) Effect of remote ischemic preconditioning on clinical outcomes in patients undergoing coronary artery bypass graft surgery (ERICCA study): a multicentre double-blind randomised controlled clinical trial. NIHR J Libr, Southampton (UK) Hausenloy DJ, Candilio L, Evans R, Ariti C, Jenkins DP, Kolvekar S, Knight R, Kunst G, Laing C, Nicholas JM, Pepper J, Robertson S, Xenou M, Clayton T, Yellon DM (2016) Effect of remote ischemic preconditioning on clinical outcomes in patients undergoing coronary artery bypass graft surgery (ERICCA study): a multicentre double-blind randomised controlled clinical trial. NIHR J Libr, Southampton (UK)
13.
Zurück zum Zitat Zhou C, Jeon Y, Meybohm P, Young PJ, Li L, Hausenloy DJ (2016) Renoprotection by remote ischemic conditioning during elective coronary revascularization: a systematic review and meta-analysis of randomized controlled trials. Int J Cardiol 222:295–302CrossRefPubMed Zhou C, Jeon Y, Meybohm P, Young PJ, Li L, Hausenloy DJ (2016) Renoprotection by remote ischemic conditioning during elective coronary revascularization: a systematic review and meta-analysis of randomized controlled trials. Int J Cardiol 222:295–302CrossRefPubMed
14.
Zurück zum Zitat Zhou C, Bulluck H, Fang N, Li L, Hausenloy DJ (2017) Age and surgical complexity impact on renoprotection by remote ischemic preconditioning during adult cardiac surgery: a meta analysis. Sci Rep 7:215CrossRefPubMedPubMedCentral Zhou C, Bulluck H, Fang N, Li L, Hausenloy DJ (2017) Age and surgical complexity impact on renoprotection by remote ischemic preconditioning during adult cardiac surgery: a meta analysis. Sci Rep 7:215CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Menting TP, Wever KE, Ozdemir-van Brunschot DM, Van der Vliet DJ, Rovers MM, Warle MC (2017) Ischaemic preconditioning for the reduction of renal ischaemia reperfusion injury. Cochrane Database Syst Rev 3:CD010777PubMed Menting TP, Wever KE, Ozdemir-van Brunschot DM, Van der Vliet DJ, Rovers MM, Warle MC (2017) Ischaemic preconditioning for the reduction of renal ischaemia reperfusion injury. Cochrane Database Syst Rev 3:CD010777PubMed
17.
Zurück zum Zitat Kork F, Eltzschig HK (2017) The devil is in the detail: remote ischemic preconditioning for perioperative kidney protection. Anestehsiology 126:763–765CrossRef Kork F, Eltzschig HK (2017) The devil is in the detail: remote ischemic preconditioning for perioperative kidney protection. Anestehsiology 126:763–765CrossRef
18.
Zurück zum Zitat Sukkar L, Hong D, Wong MG, Badve SV, Rogers K, Perkovic V, Walsh M, Yu X, Hillis GS, Gallagher M, Jardine M (2016) Effects of ischaemic conditioning on major clinical outcomes in people undergoing invasive procedures: systematic review and meta-analysis. BMJ 355:i5599CrossRefPubMedPubMedCentral Sukkar L, Hong D, Wong MG, Badve SV, Rogers K, Perkovic V, Walsh M, Yu X, Hillis GS, Gallagher M, Jardine M (2016) Effects of ischaemic conditioning on major clinical outcomes in people undergoing invasive procedures: systematic review and meta-analysis. BMJ 355:i5599CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Zhang Y, Zhang X, Chi D, Wang S, Wei H, Yu H, Li Q, Liu B (2016) Remote ischemic preconditioning for prevention of acute kidney injury in patients undergoing on-pump cardiac surgery: a systematic review and meta-analysis. Medicine (Baltimore) 95:e3465CrossRef Zhang Y, Zhang X, Chi D, Wang S, Wei H, Yu H, Li Q, Liu B (2016) Remote ischemic preconditioning for prevention of acute kidney injury in patients undergoing on-pump cardiac surgery: a systematic review and meta-analysis. Medicine (Baltimore) 95:e3465CrossRef
20.
Zurück zum Zitat Bei WJ, Duan CY, Chen JY, Wang K, Liu YH, Kiu Y, Tan N (2016) Remote ischemic conditioning for preventing contrast-induced acute kidney injury in patients undergoing percutaneous coronary interventions/coronary angiography: a meta-analysis of randomized controlled trials. J Cardiovasc Pharmacol Ther 21:53–63CrossRefPubMed Bei WJ, Duan CY, Chen JY, Wang K, Liu YH, Kiu Y, Tan N (2016) Remote ischemic conditioning for preventing contrast-induced acute kidney injury in patients undergoing percutaneous coronary interventions/coronary angiography: a meta-analysis of randomized controlled trials. J Cardiovasc Pharmacol Ther 21:53–63CrossRefPubMed
21.
Zurück zum Zitat Michaely HJ, Metzger L, Haneder S, Hansmann J, Schoenberg SO, Attenberger UI (2012) Renal BOLD-MRI does not reflect renal function in chronic kidney disease. Kidney Int 81:684–689CrossRefPubMed Michaely HJ, Metzger L, Haneder S, Hansmann J, Schoenberg SO, Attenberger UI (2012) Renal BOLD-MRI does not reflect renal function in chronic kidney disease. Kidney Int 81:684–689CrossRefPubMed
22.
Zurück zum Zitat Prasad PV, Edelman RR, Epstein FH (1996) Noninvasive evaluation of intrarenal oxygenation with BOLD MRI. Circulation 94:3271–3275CrossRefPubMed Prasad PV, Edelman RR, Epstein FH (1996) Noninvasive evaluation of intrarenal oxygenation with BOLD MRI. Circulation 94:3271–3275CrossRefPubMed
23.
Zurück zum Zitat Li LP, Thacker J, Lu J, Franklin T, Zhou Y, Papadopulou MV, Solomon R, Prasad PV (2014) Efficacy of preventive interventions for iodinated contrast-induced acute kidney injury evaluated by intrarenal oxygenation as an early marker. Invest Radiol 49:647–652CrossRefPubMedPubMedCentral Li LP, Thacker J, Lu J, Franklin T, Zhou Y, Papadopulou MV, Solomon R, Prasad PV (2014) Efficacy of preventive interventions for iodinated contrast-induced acute kidney injury evaluated by intrarenal oxygenation as an early marker. Invest Radiol 49:647–652CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Vinten-Johansen J, Yellon DM, Opie LH (2005) Postconditioning: a simple, clinically applicable procedure to improve revascularization in acute myocardial infarction. Circulation 112:2085–2088CrossRefPubMed Vinten-Johansen J, Yellon DM, Opie LH (2005) Postconditioning: a simple, clinically applicable procedure to improve revascularization in acute myocardial infarction. Circulation 112:2085–2088CrossRefPubMed
25.
Zurück zum Zitat Kin H, Zhao ZQ, Sun HY, Wang NP, Corvera JS, Halkos ME, Kerendi F, Guyton RA, Vinten-Johansen J (2004) Postconditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion. Cardiovasc Res 62:74–85CrossRefPubMed Kin H, Zhao ZQ, Sun HY, Wang NP, Corvera JS, Halkos ME, Kerendi F, Guyton RA, Vinten-Johansen J (2004) Postconditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion. Cardiovasc Res 62:74–85CrossRefPubMed
26.
Zurück zum Zitat Lang SC, Elsasser A, Scheler C, Vetter S, Tiefenbacher CP, Kubler W, Katus HA, Vogt AM (2006) Myocardial preconditioning and remote renal preconditioning: identifying a protective factor using proteomic methods? Basic Res Cardiol 101:149–158CrossRefPubMed Lang SC, Elsasser A, Scheler C, Vetter S, Tiefenbacher CP, Kubler W, Katus HA, Vogt AM (2006) Myocardial preconditioning and remote renal preconditioning: identifying a protective factor using proteomic methods? Basic Res Cardiol 101:149–158CrossRefPubMed
27.
Zurück zum Zitat Olenchock BA, Moslehi J, Baik AH, Davidson SM, Williams J, Gibson WJ, Chakraborty AA, Pierce KA, Miller CM, Hanse EA, Kelekar A, Sullivan LB, Wagers AJ, Clish CB, Vander Heiden MG, Kaelin WG Jr (2016) EGLN1 inhibition and rerouting of α-ketoglutarate suffice for remote ischemic protection. Cell 164:884–895CrossRefPubMedPubMedCentral Olenchock BA, Moslehi J, Baik AH, Davidson SM, Williams J, Gibson WJ, Chakraborty AA, Pierce KA, Miller CM, Hanse EA, Kelekar A, Sullivan LB, Wagers AJ, Clish CB, Vander Heiden MG, Kaelin WG Jr (2016) EGLN1 inhibition and rerouting of α-ketoglutarate suffice for remote ischemic protection. Cell 164:884–895CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Brezis M, Rosen S (1995) Hypoxia of the renal medulla—it’s implications for disease. N Engl J Med 332:647–655CrossRefPubMed Brezis M, Rosen S (1995) Hypoxia of the renal medulla—it’s implications for disease. N Engl J Med 332:647–655CrossRefPubMed
29.
Zurück zum Zitat Persson PB, Hansell P, Liss P (2005) Pathophysiology of contrast medium-induced nephropathy. Kidney Int 68:14–22CrossRefPubMed Persson PB, Hansell P, Liss P (2005) Pathophysiology of contrast medium-induced nephropathy. Kidney Int 68:14–22CrossRefPubMed
30.
Zurück zum Zitat Geenen RW, Kingma HJ, van der Molen AJ (2013) Contrast-induced nephropathy: pharmacology, pathophysiology and prevention. Insights Imaging 4:811–820CrossRefPubMedPubMedCentral Geenen RW, Kingma HJ, van der Molen AJ (2013) Contrast-induced nephropathy: pharmacology, pathophysiology and prevention. Insights Imaging 4:811–820CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Wang JH, Ren K, Sun WG, Zhao L, Zhong HS, Xu K (2014) Effects of iodinated contrast agents on renal oxygenation level determined by blood oxygenation level dependent magnetic resonance imaging in rabbit models of type 1 and type 2 diabetic nephropathy. BMC Nephrol 15:140CrossRefPubMedPubMedCentral Wang JH, Ren K, Sun WG, Zhao L, Zhong HS, Xu K (2014) Effects of iodinated contrast agents on renal oxygenation level determined by blood oxygenation level dependent magnetic resonance imaging in rabbit models of type 1 and type 2 diabetic nephropathy. BMC Nephrol 15:140CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Zhang Y, Wang J, Yang X, Wang X, Zhang J, Fang J, Jiang X (2012) The serial effect of iodinated contrast media on renal hemodynamics and oxygenation as evaluated by ASL and BOLD MRI. Contrast Media Mol Imaging 7:418–425CrossRefPubMed Zhang Y, Wang J, Yang X, Wang X, Zhang J, Fang J, Jiang X (2012) The serial effect of iodinated contrast media on renal hemodynamics and oxygenation as evaluated by ASL and BOLD MRI. Contrast Media Mol Imaging 7:418–425CrossRefPubMed
33.
Zurück zum Zitat Pedersen M, Dissing TH, Morkenborg J, Stodkilde-Jorgensen H, Hansen LH, Pedersen LB, Grenier N, Frokiaer J (2005) Validation of quantitative BOLD MRI measurements in kidney: application to unilateral ureteral obstruction. Kidney Int 67:2305–2312CrossRefPubMed Pedersen M, Dissing TH, Morkenborg J, Stodkilde-Jorgensen H, Hansen LH, Pedersen LB, Grenier N, Frokiaer J (2005) Validation of quantitative BOLD MRI measurements in kidney: application to unilateral ureteral obstruction. Kidney Int 67:2305–2312CrossRefPubMed
34.
Zurück zum Zitat Tumkur SM, Vu AT, Li LP, Pierchala L, Prasad PV (2006) Evaluation of intra-renal oxygenation during water diuresis: a time-resolved study using BOLD MRI. Kidney Int 70:139–143CrossRefPubMedPubMedCentral Tumkur SM, Vu AT, Li LP, Pierchala L, Prasad PV (2006) Evaluation of intra-renal oxygenation during water diuresis: a time-resolved study using BOLD MRI. Kidney Int 70:139–143CrossRefPubMedPubMedCentral
35.
Metadaten
Titel
Assessing renal changes after remote ischemic preconditioning (RIPC) of the upper extremity using BOLD imaging at 3T
verfasst von
Florian Siedek
Thorsten Persigehl
Roman-Ulrich Mueller
Volker Burst
Thomas Benzing
David Maintz
Stefan Haneder
Publikationsdatum
01.06.2018
Verlag
Springer International Publishing
Erschienen in
Magnetic Resonance Materials in Physics, Biology and Medicine / Ausgabe 3/2018
Print ISSN: 0968-5243
Elektronische ISSN: 1352-8661
DOI
https://doi.org/10.1007/s10334-017-0658-4

Weitere Artikel der Ausgabe 3/2018

Magnetic Resonance Materials in Physics, Biology and Medicine 3/2018 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.