Ischemic preconditioning at a remote site prevents acute kidney injury in patients following cardiac surgery
2011; Elsevier BV; Volume: 80; Issue: 8 Linguagem: Inglês
10.1038/ki.2011.156
ISSN1523-1755
AutoresRobert F. Zimmerman, Prosperity U. Ezeanuna, Jane Kane, Catherine D. Cleland, Thejaswini J. Kempananjappa, F. Lee Lucas, Robert S. Kramer,
Tópico(s)Anesthesia and Neurotoxicity Research
ResumoAcute kidney injury, a common complication of cardiac surgery with cardiopulmonary bypass, is associated with increased morbidity and mortality. Ischemic preconditioning at a remote site mitigates ischemia–reperfusion injury and may prevent acute kidney injury after cardiac surgery, thus providing clinical benefit. To further study this, we enrolled 120 adult patients undergoing elective cardiac surgery for whom cardiopulmonary bypass was anticipated in a randomized, single-blind, and controlled pilot trial. Patients were stratified for the type of surgery and equally assigned to a control group or to receive remote ischemic preconditioning by an automated thigh tourniquet consisting of three 5-min intervals of lower extremity ischemia separated by 5-min intervals of reperfusion. The primary end point was acute kidney injury defined as an elevation of serum creatinine of ≥0.3 mg/dl or ≥50% within 48 h after surgery. Fifty-nine patients in each group were analyzed on an intention-to-treat basis. Acute kidney injury occurred in 12 remote ischemic preconditioned and 28 control patients, reflecting an absolute risk reduction of 0.27 and a significantly reduced relative risk due to preconditioning of 0.43. Hence, remote ischemic preconditioning prevents acute kidney injury in patients undergoing cardiopulmonary bypass-assisted cardiac surgery. Acute kidney injury, a common complication of cardiac surgery with cardiopulmonary bypass, is associated with increased morbidity and mortality. Ischemic preconditioning at a remote site mitigates ischemia–reperfusion injury and may prevent acute kidney injury after cardiac surgery, thus providing clinical benefit. To further study this, we enrolled 120 adult patients undergoing elective cardiac surgery for whom cardiopulmonary bypass was anticipated in a randomized, single-blind, and controlled pilot trial. Patients were stratified for the type of surgery and equally assigned to a control group or to receive remote ischemic preconditioning by an automated thigh tourniquet consisting of three 5-min intervals of lower extremity ischemia separated by 5-min intervals of reperfusion. The primary end point was acute kidney injury defined as an elevation of serum creatinine of ≥0.3 mg/dl or ≥50% within 48 h after surgery. Fifty-nine patients in each group were analyzed on an intention-to-treat basis. Acute kidney injury occurred in 12 remote ischemic preconditioned and 28 control patients, reflecting an absolute risk reduction of 0.27 and a significantly reduced relative risk due to preconditioning of 0.43. Hence, remote ischemic preconditioning prevents acute kidney injury in patients undergoing cardiopulmonary bypass-assisted cardiac surgery. Acute kidney injury, a significant complication of cardiac surgery, is occurring with greater frequency as patients at high risk for complications are increasingly referred for surgery.1.Thakar C.V. Worley S. Arrigain S. et al.Improved survival in acute kidney injury after cardiac surgery.Am J Kidney Dis. 2007; 50: 703-711Abstract Full Text Full Text PDF PubMed Scopus (82) Google Scholar, 2.Baillot R.G. Joanisse D.R. Stevens L.M. et al.Recent evolution in demographic and clinical characteristics and in-hospital morbidity in patients undergoing coronary surgery.Can J Surg. 2009; 52: 394-400PubMed Google Scholar Depending on how it is defined, acute kidney injury occurs in up to 45% of patients after cardiac surgery, and approximately 1 to 2% require renal replacement therapy.3.Chertow G.M. Lazarus J.M. Christiansen C.L. et al.Preoperative renal risk stratification.Circulation. 1997; 95: 878-884Crossref PubMed Scopus (663) Google Scholar, 4.Koyner J.L. Bennett M.R. 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Diamondstone L.S. Ramsay J.G. et al.Renal dysfunction after myocardial revascularization: risk factors, adverse outcomes, and hospital resource utilization. The Multicenter Study of Perioperative Ischemia Research Group.Ann Intern Med. 1998; 128: 194-203Crossref PubMed Scopus (929) Google Scholar, 7.Ryckwaert F. Boccara G. Frappier J.M. et al.Incidence, risk factors, and prognosis of a moderate increase in plasma creatinine early after cardiac surgery.Crit Care Med. 2002; 30: 1495-1498Crossref PubMed Scopus (133) Google Scholar, 8.Lassnigg A. Schmidlin D. Mouhieddine M. et al.Minimal changes of serum creatinine predict prognosis in patients after cardiothoracic surgery: a prospective cohort study.J Am Soc Nephrol. 2004; 15: 1597-1605Crossref PubMed Scopus (1090) Google Scholar, 9.Loef B.G. Epema A.H. 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Saczkowski R.S. et al.A small post-operative rise in serum creatinine predicts acute kidney injury in children undergoing cardiac surgery.Kidney Int. 2009; 76: 885-892Abstract Full Text Full Text PDF PubMed Scopus (246) Google Scholar Recognizing that even small increases in serum creatinine levels are associated with increased morbidity and mortality, the Acute Kidney Injury Network (AKIN) has recommended an acute increase in the serum creatinine concentration of ≥0.3 mg/dl as a diagnostic criterion for acute kidney injury.12.Mehta R.L. Kellum J.A. Shah S.V. et al.Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury.Crit Care. 2007; 11: R31Crossref PubMed Scopus (5228) Google Scholar Cardiopulmonary bypass is employed in most cardiac surgeries, and although the mechanisms are not fully understood, ensuing ischemic, inflammatory, and oxidative injuries to renal tubular epithelial cells have been implicated in the cause of acute kidney injury.13.Rosner M.H. Okusa M.D. Acute kidney injury associated with cardiac surgery.Clin J Am Soc Nephrol. 2006; 1: 19-32Crossref PubMed Scopus (822) Google Scholar Despite numerous clinical trials of pharmacologic interventions, a means to prevent acute kidney injury associated with cardiac surgery has remained elusive.13.Rosner M.H. Okusa M.D. Acute kidney injury associated with cardiac surgery.Clin J Am Soc Nephrol. 2006; 1: 19-32Crossref PubMed Scopus (822) Google Scholar, 14.Burns K.E. Chu M.W. Novick R.J. et al.Perioperative N-acetylcysteine to prevent renal dysfunction in high-risk patients undergoing CABG surgery: a randomized controlled trial.JAMA. 2005; 294: 342-350Crossref PubMed Scopus (184) Google Scholar, 15.Young E.W. Diab A. Kirsh M.M. Intravenous diltiazem and acute renal failure after cardiac operations.Ann Thorac Surg. 1998; 65: 1316-1319Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar, 16.Ranucci M. Soro G. Barzaghi N. et al.Fenoldopam prophylaxis of postoperative acute renal failure in high-risk cardiac surgery patients.Ann Thorac Surg. 2004; 78 (discussion 1337–1338): 1332-1337Abstract Full Text Full Text PDF PubMed Scopus (76) Google Scholar Remote ischemic preconditioning is a phenomenon in which ischemia–reperfusion injury of an organ is mitigated by previous application of brief ischemic intervals in a distant organ or limb.17.Gho B.C. Schoemaker R.G. van den Doel M.A. et al.Myocardial protection by brief ischemia in noncardiac tissue.Circulation. 1996; 94: 2193-2200Crossref PubMed Scopus (534) Google Scholar, 18.Birnbaum Y. Hale S.L. Kloner R.A. Ischemic preconditioning at a distance: reduction of myocardial infarct size by partial reduction of blood supply combined with rapid stimulation of the gastrocnemius muscle in the rabbit.Circulation. 1997; 96: 1641-1646Crossref PubMed Scopus (332) Google Scholar Several encouraging trials of remote ischemic preconditioning have suggested clinical benefit.19.Cheung M.M. Kharbanda R.K. Konstantinov I.E. et al.Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans.J Am Coll Cardiol. 2006; 47: 2277-2282Abstract Full Text Full Text PDF PubMed Scopus (460) Google Scholar, 20.Hausenloy D.J. Mwamure P.K. Venugopal V. et al.Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial.Lancet. 2007; 370: 575-579Abstract Full Text Full Text PDF PubMed Scopus (554) Google Scholar, 21.Ali Z.A. Callaghan C.J. Lim E. et al.Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial.Circulation. 2007; 116: I98-105Crossref PubMed Scopus (386) Google Scholar, 22.Hoole S.P. Heck P.M. Sharples L. et al.Cardiac Remote Ischemic Preconditioning in Coronary Stenting (CRISP Stent) Study: a prospective, randomized control trial.Circulation. 2009; 119: 820-827Crossref PubMed Scopus (369) Google Scholar, 23.Venugopal V. Hausenloy D.J. Ludman A. et al.Remote ischaemic preconditioning reduces myocardial injury in patients undergoing cardiac surgery with cold-blood cardioplegia: a randomised controlled trial.Heart. 2009; 95: 1567-1571Crossref PubMed Scopus (197) Google Scholar, 24.Bøtker H.E. Kharbanda R. Schmidt M.R. et al.Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial.Lancet. 2010; 375: 727-734Abstract Full Text Full Text PDF PubMed Scopus (811) Google Scholar, 25.Venugopal V. Laing C.M. Ludman A. et al.Effect of remote ischemic preconditioning on acute kidney injury in nondiabetic patients undergoing coronary artery bypass graft surgery: a secondary analysis of 2 small randomized trials.Am J Kidney Dis. 2010; 56: 1043-1049Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar Because the mechanisms of ischemia–reperfusion injury26.Bonventre J.V. Zuk A. Ischemic acute renal failure: an inflammatory disease?.Kidney Int. 2004; 66: 480-485Abstract Full Text Full Text PDF PubMed Scopus (627) Google Scholar, 27.Yellon D.M. Hausenloy D.J. Myocardial reperfusion injury.N Engl J Med. 2007; 357: 1121-1135Crossref PubMed Scopus (2822) Google Scholar are similar to those proposed for acute kidney injury after cardiopulmonary bypass, we tested the hypothesis that remote ischemic preconditioning prevents acute kidney injury in patients undergoing cardiac surgery. We randomized 120 patients to remote ischemic preconditioning (n=60) and control (n=60) groups: 79 scheduled for coronary artery bypass grafting (CABG), 18 for valve surgery, and 23 for combined CABG and valve or other surgery (Figure 1). When scheduled and actual surgeries were different, actual surgeries were used for the intention-to-treat and per-protocol analyses. One CABG patient was randomized from a block used out of sequence. After exclusion of 2 patients (1 remote ischemic preconditioning patient and 1 control patient for whom second postoperative day serum creatinine levels were not obtained), 59 patients in each group were included in the intention-to-treat analysis. Two patients who underwent CABG without cardiopulmonary bypass were excluded in the per-protocol analysis. The remote ischemic preconditioning and control groups were not significantly different with respect to baseline characteristics (Table 1) and operative data (Table 2), except that more patients in the control group had a history of previous cardiac surgery. Prediction scores for acute kidney injury requiring renal replacement therapy were similar between groups, as were the proportions of patients at moderate or high risk (score >2).Table 1Baseline characteristics of the study patients according to intervention groupRIPC (n=59)Control (n=59)P-valueAge, year62±9aThe ± values are means±s.d.65±110.14Male sex, no. (%)41 (69)40 (68)0.84Preoperative creatinine, mg/dlbTo convert values for creatinine to μmol/l, multiply by 88.4.0.93±0.240.95±0.310.68GFR <60 ml/min per 1.73 m2, no. (%)cGFR is calculated by a simplified Modification of Diet in Renal Disease (MDRD) formula.10 (17)9 (15)0.80Comorbidities Hypertension, no. (%)44 (75)50 (85)0.25 Diabetes mellitus24 (41)21 (36)0.70Insulin requiring, no. (%)9 (15)5 (8)0.39 Congestive heart failure, no. (%)10 (17)9 (15)0.80 Peripheral vascular disease, no. (%)8 (14)10 (17)0.80 Chronic obstructive pulmonary disease, no. (%)11 (19)5 (8)0.18Previous heart surgery, no. (%)6 (10)15 (25)0.05Left ventricular ejection fraction 48 h, no. (%)3 (5)4 (7)>0.99dFisher's exact test. Reintubation, no. (%)2 (3)2 (3)—Complications Myocardial infarction0 (0)0 (0)— Congestive heart failure1 (2)0 (0)>0.99dFisher's exact test.Hospital outcomes ICU stay >3 days, no. (%)12 (20)8 (14)0.46 Hospital stay after surgery, daysbReported as median (range).7 (3, 35)6 (4, 49)0.39cMann–Whitney U test. Hospital death, no. (%)0 (0)1 (2)>0.99dFisher's exact test.Abbreviations: AKI, acute kidney injury; AKIN, Acute Kidney Injury Network; ICU, intensive care unit; MV, mechanical ventilation; NGAL, neutrophil gelatinase-associated lipocalin, RIFLE, risk, injury, failure, loss, and end-stage disease; RIPC, remote ischemic preconditioning; RRT, renal replacement therapy.a NGAL data were analyzed for 53 RIPC patients and 55 control patients. Oliguria data were analyzed for 56 RIPC patients and 57 control patients.b Reported as median (range).c Mann–Whitney U test.d Fisher's exact test. Open table in a new tab Abbreviations: AKI, acute kidney injury; AKIN, Acute Kidney Injury Network; ICU, intensive care unit; MV, mechanical ventilation; NGAL, neutrophil gelatinase-associated lipocalin, RIFLE, risk, injury, failure, loss, and end-stage disease; RIPC, remote ischemic preconditioning; RRT, renal replacement therapy. Because significantly more patients in the control group than in the intervention group had a history of previous cardiac surgery, we performed an additional χ2 analysis stratified on previous cardiac surgery history, with nearly identical results (relative risk, 0.45; P=0.004). Median change in plasma neutrophil gelatinase-associated lipocalin (NGAL) levels, drawn immediately before the preconditioning regimen and 3 h after cardiopulmonary bypass, did not differ significantly between the remote ischemic preconditioning and control groups (39 vs 43 ng/ml, respectively; P=0.46). We observed a nonsignificant difference in the incidence of postoperative oliguria during the initial 12 h after surgery between remote ischemic preconditioning and control groups (7% vs 2%, respectively; P=0.36; Table 3). Per-protocol analysis remained nonsignificant for both outcomes (data not shown). In a post hoc analysis of patients who had acute kidney injury, 11 (19%) and 23 (39%) patients had stage I acute kidney injury, and 1 (2%) and 5 (8%) patients had stage II acute kidney injury in the remote ischemic preconditioning and control groups, respectively (P=0.005; Table 3). No patients had stage III acute kidney injury within the first postoperative 48 h or required renal replacement therapy before hospital discharge. Significantly fewer patients in the remote ischemic preconditioning group had sustained acute kidney injury for at least 2 consecutive days compared with the control group (17% vs 36%; P=0.04). Sustained acute kidney injury for at least 3 consecutive days occurred less frequently in the remote ischemic preconditioning group (8% vs 19%), but this difference was not statistically significant (P=0.18; Table 3). We found no significant differences between groups in the use of vasoactive drugs, prolonged mechanical ventilation, or need for reintubation. No patients had postoperative myocardial infarction. One patient in the remote ischemic preconditioning group had postoperative congestive heart failure. Length of intensive care unit stay and hospital stay after surgery were comparable. One patient in the control group died 2 days after surgery (Table 3). Our study shows that remote ischemic preconditioning prevents acute kidney injury in patients undergoing cardiac surgery with cardiopulmonary bypass. We observed a 27% absolute risk reduction in the primary end point of an acute increase in serum creatinine levels by at least 0.3 mg/dl or 50% more than the baseline value within 48 h of surgery. Sustained acute kidney injury in which serum creatinine levels remained elevated for at least 2 consecutive days was also significantly reduced in the remote ischemic preconditioning group. Several studies have described an association between acute kidney injury and increased morbidity, short-term and long-term mortality, and use of resources in various patient populations.3.Chertow G.M. Lazarus J.M. Christiansen C.L. et al.Preoperative renal risk stratification.Circulation. 1997; 95: 878-884Crossref PubMed Scopus (663) Google Scholar, 5.Hobson C.E. Yavas S. Segal M.S. et al.Acute kidney injury is associated with increased long-term mortality after cardiothoracic surgery.Circulation. 2009; 119: 2444-2453Crossref PubMed Scopus (695) Google Scholar, 6.Mangano C.M. Diamondstone L.S. Ramsay J.G. et al.Renal dysfunction after myocardial revascularization: risk factors, adverse outcomes, and hospital resource utilization. The Multicenter Study of Perioperative Ischemia Research Group.Ann Intern Med. 1998; 128: 194-203Crossref PubMed Scopus (929) Google Scholar, 7.Ryckwaert F. Boccara G. Frappier J.M. et al.Incidence, risk factors, and prognosis of a moderate increase in plasma creatinine early after cardiac surgery.Crit Care Med. 2002; 30: 1495-1498Crossref PubMed Scopus (133) Google Scholar, 8.Lassnigg A. Schmidlin D. Mouhieddine M. et al.Minimal changes of serum creatinine predict prognosis in patients after cardiothoracic surgery: a prospective cohort study.J Am Soc Nephrol. 2004; 15: 1597-1605Crossref PubMed Scopus (1090) Google Scholar, 9.Loef B.G. Epema A.H. Smilde T.D. et al.Immediate postoperative renal function deterioration in cardiac surgical patients predicts in-hospital mortality and long-term survival.J Am Soc Nephrol. 2005; 16: 195-200Crossref PubMed Scopus (387) Google Scholar, 10.Dasta J.F. Kane-Gill S.L. Durtschi A.J. et al.Costs and outcomes of acute kidney injury (AKI) following cardiac surgery.Nephrol Dial Transplant. 2008; 23: 1970-1974Crossref PubMed Scopus (292) Google Scholar, 11.Zappitelli M. Bernier P.L. Saczkowski R.S. et al.A small post-operative rise in serum creatinine predicts acute kidney injury in children undergoing cardiac surgery.Kidney Int. 2009; 76: 885-892Abstract Full Text Full Text PDF PubMed Scopus (246) Google Scholar, 28.Parikh C.R. Coca S.G. Wang Y. et al.Long-term prognosis of acute kidney injury after acute myocardial infarction.Arch Intern Med. 2008; 168: 987-995Crossref PubMed Scopus (260) Google Scholar, 29.Lafrance J.P. Miller D.R. Acute kidney injury associates with increased long-term mortality.J Am Soc Nephrol. 2010; 21: 345-352Crossref PubMed Scopus (432) Google Scholar, 30.Chertow G.M. Burdick E. Honour M. et al.Acute kidney injury, mortality, length of stay, and costs in hospitalized patients.J Am Soc Nephrol. 2005; 16: 3365-3370Crossref PubMed Scopus (2502) Google Scholar These relationships hold true even with small increases of serum creatinine levels for hospital inpatients and patients who have undergone cardiac surgery.5.Hobson C.E. Yavas S. Segal M.S. et al.Acute kidney injury is associated with increased long-term mortality after cardiothoracic surgery.Circulation. 2009; 119: 2444-2453Crossref PubMed Scopus (695) Google Scholar, 7.Ryckwaert F. Boccara G. Frappier J.M. et al.Incidence, risk factors, and prognosis of a moderate increase in plasma creatinine early after cardiac surgery.Crit Care Med. 2002; 30: 1495-1498Crossref PubMed Scopus (133) Google Scholar, 8.Lassnigg A. Schmidlin D. Mouhieddine M. et al.Minimal changes of serum creatinine predict prognosis in patients after cardiothoracic surgery: a prospective cohort study.J Am Soc Nephrol. 2004; 15: 1597-1605Crossref PubMed Scopus (1090) Google Scholar, 9.Loef B.G. Epema A.H. Smilde T.D. et al.Immediate postoperative renal function deterioration in cardiac surgical patients predicts in-hospital mortality and long-term survival.J Am Soc Nephrol. 2005; 16: 195-200Crossref PubMed Scopus (387) Google Scholar, 28.Parikh C.R. Coca S.G. Wang Y. et al.Long-term prognosis of acute kidney injury after acute myocardial infarction.Arch Intern Med. 2008; 168: 987-995Crossref PubMed Scopus (260) Google Scholar, 30.Chertow G.M. Burdick E. Honour M. et al.Acute kidney injury, mortality, length of stay, and costs in hospitalized patients.J Am Soc Nephrol. 2005; 16: 3365-3370Crossref PubMed Scopus (2502) Google Scholar Moreover, the associations persist after adjustment for comorbidities and other factors predisposing to acute kidney injury, suggesting that even mild and clinically transient acute kidney injury has lasting effects on patient survival rather than simply being a marker for comorbidities and other contributors to mortality. Establishment of a method to prevent acute kidney injury in at-risk patients could substantially improve health outcomes. Remote ischemic preconditioning has shown promise in randomized, controlled trials as a means for myocardial protection during coronary bypass surgery,20.Hausenloy D.J. Mwamure P.K. Venugopal V. et al.Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial.Lancet. 2007; 370: 575-579Abstract Full Text Full Text PDF PubMed Scopus (554) Google Scholar, 23.Venugopal V. Hausenloy D.J. Ludman A. et al.Remote ischaemic preconditioning reduces myocardial injury in patients undergoing cardiac surgery with cold-blood cardioplegia: a randomised controlled trial.Heart. 2009; 95: 1567-1571Crossref PubMed Scopus (197) Google Scholar surgical repair of congenital heart defects,19.Cheung M.M. Kharbanda R.K. Konstantinov I.E. et al.Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans.J Am Coll Cardiol. 2006; 47: 2277-2282Abstract Full Text Full Text PDF PubMed Scopus (460) Google Scholar and before percutaneous coronary interventions.22.Hoole S.P. Heck P.M. Sharples L. et al.Cardiac Remote Ischemic Preconditioning in Coronary Stenting (CRISP Stent) Study: a prospective, randomized control trial.Circulation. 2009; 119: 820-827Crossref PubMed Scopus (369) Google Scholar, 24.Bøtker H.E. Kharbanda R. Schmidt M.R. et al.Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial.Lancet. 2010; 375: 727-734Abstract Full Text Full Text PDF PubMed Scopus (811) Google Scholar Two studies have reported a protective effect of remote ischemic preconditioning on renal function. In a randomized, controlled trial, Ali et al.21.Ali Z.A. Callaghan C.J. Lim E. et al.Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial.Circulation. 2007; 116: I98-105Crossref PubMed Scopus (386) Google Scholar observed a relative risk for postoperative 'renal impairment' (that is, serum creatinine level >2.0 mg/dl) of 0.25 in patients who had undergone abdominal aortic aneurysm repair and received preconditioning before surgery. Venugopal et al.25.Venugopal V. Laing C.M. Ludman A. et al.Effect of remote ischemic preconditioning on acute kidney injury in nondiabetic patients undergoing coronary artery bypass graft surgery: a secondary analysis of 2 small randomized trials.Am J Kidney Dis. 2010; 56: 1043-1049Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar retrospectively analyzed two randomized controlled trials of remote ischemic preconditioning for myocardial protection during coronary artery bypass graft surgery. The relative risk for acute kidney injury, defined by AKIN criteria, in patients who received the preconditioning regimen was 0.42, a finding of marginal statistical significance (P=0.10). In contrast to our findings and those of Ali et al.21.Ali Z.A. Callaghan C.J. Lim E. et al.Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial.Circulation. 2007; 116: I98-105Crossref PubMed Scopus (386) Google Scholar and Venugopal et al.,25.Venugopal V. Laing C.M. Ludman A. et al.Effect of remote ischemic preconditioning on acute kidney injury in nondiabetic patients undergoing coronary artery bypass graft surgery: a secondary analysis of 2 small randomized trials.Am J Kidney Dis. 2010; 56: 1043-1049Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar a randomized controlled trial of remote ischemic preconditioning in 162 patients undergoing coronary artery bypass graft surgery while on cardiopulmonary bypass failed to demonstrate renal protection with preconditioning.31.Rahman I.A. Mascaro J.G. Steeds R.P. et al.Remote ischemic preconditioning in human coronary artery bypass surgery: from promise to disappointment?.Circulation. 2010; 122: S53-S59Crossref PubMed Scopus (221) Google Scholar Postoperative serum creatinine was not measured until the fourth day following surgery. A protective effect of remote ischemic preconditioning on renal f
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