Is Timing Everything?
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1 The Journal of ExtraCorporeal Technology Is Timing Everything? George Justison, CCP University of Colorado Hospital, Perfusion Services, Aurora, Colorado Presented at Goal Directed Therapy Symposium, 54th AmSECT International Conference, Colorado Springs, Colorado, March 19, Thank you Ben and AmSECT for organizing this conference. And thank you all for showing up on Saturday morning. My objectives for this presentation are to review the current knowledge of time spent below critical thresholds and more specifically the relationship between low oxygen delivery and organ function following cardiopulmonary bypass (CPB). Additionally, we will investigate the time dose relationship between goal-directed perfusion (GDP) parameters and acute kidney injury (AKI). Here are my disclosures. [Slide: I have received speaker honorariums from LivaNova. I have no conflicts of interest for this presentation]. I did not conspire with Bob (Groom) to bring up Galletti, but it s important for us to remember our history, otherwise, as they say, we re doomed to repeat it. Galletti, was the first textbook on CPB published in In that book, there is an entire chapter on perfusion adequacy. In the summation of that chapter, he says that the ultimate aim of perfusion is to provide satisfactory tissue gas exchange (1). What we re measuring with GDP is tissue gas exchange. The other quote from Galletti that I didn t show, from that same chapter, is that each organism is in their own control. Each organism, if we measure respiratory tissue gas exchange on bypass, will tell us exactly what they need or define their own unique critical threshold for oxygen delivery. How do we describe adequate perfusion? In conventional terms, many of us were taught and practice to include multiple facets of not only delivery of blood flow but also the patient s response to perfusion. That may include elements such as venous saturation monitoring or venous po 2 monitoring. It certainly includes maintaining an adequate ph during CPB, arterial pco 2 measurement, and monitoring blood flow or cardiac index, typically in the range of Address correspondence to: George Justison, CCP, University of Colorado Hospital, Perfusion Services, E. 16th Avenue, Aurora, CO george.justison@uchealth.org during normothermia. Some adjustment may be based on temperature. As we saw in the audience response survey, some of us even include lactate monitoring in that measure of perfusion adequacy. When we discuss GDP, many perfusionists are initially worried that they have to give up everything that they have practiced as an adequate measure of perfusion, and that s not what this concept is about. GDP is about enhancing our current knowledge of adequate perfusion and using respiratory-based parameters to give us a whole new level of detail of what s happening to the patient on a tissue level. In GDP, we take conventional terms of perfusion adequacy and we add to it concepts of cellular respiration, including oxygen delivery index (DO 2 i), oxygen consumption index (VO 2 i), and carbon dioxide production index (VCO 2 i). Instead of isolated elements like blood flow, hematocrit, and global measures of oxygen utilization like SvO 2 and PvO 2, we now describe blood flow as DO 2 i, the product of blood flow and hemoglobin. We can monitor how that patient is using the delivered oxygen as the oxygen consumption index (VO 2 i). And more importantly, the end product of that oxygen utilization the carbon dioxide production index (VCO 2 i), which includes elements of aerobic and anaerobic respiration (Table 1). Equally importantly in our management is the relationship of these different parameters to each other. Important relationships in GDP include the oxygen delivery index to carbon dioxide production index ratio (DO 2 i/vco 2 i). The DO 2 i/vco 2 i ratio tells us if the oxygen delivery is adequate for the current metabolic rate of the patient. We also look at the oxygen consumption to oxygen delivery index or the oxygen extraction ratio (VO 2 i/do 2 i). How much of that delivered oxygen is the patient removing and using. A new concept for many of us, but one that Dr. Rivers pointed out earlier in his work on resuscitation of patients, is the respiratory quotient. The respiratory quotient is the ratio of CO 2 production index to the oxygen consumption index (VCO 2 i/vo 2 i). And as we re learning more about P13
2 P14 G. JUSTISON Table 1. Common conventional terms to describe adequacy of perfusion on CPB compared to additional GDP terms of adequate CPB. Conventional CPB Terms GDP Terms SvO 2 >60 70% Oxygen delivery index (DO 2 i) PvO 2 >40mmHg Oxygen consumption index (VO 2 i) ph = Carbon dioxide production index (VCO 2 i) pco 2 =32 42 mm Hg DO 2 i/vco 2 i Cardiac index = l/min/m 2 VO 2 i/do 2 i Lactate < 2.0 mmol/l VCO 2 i/vo 2 i GDP, we re finding out that the respiratory quotient is a very important parameter. Considering that our goal is to talk about respiration on CPB, I probably should have retitled my talk as How Long Can You Hold Your Breath before Bad Things Start to Happen. In 1992, Shoemaker published a paper describing the role of intraoperative oxygen debt on survival in high-risk surgical patients (2). In surgical patients who occur an oxygen debt, in our case specifically during cardiac surgery, there is a window of time in which the incurred oxygen debt must be replaced without developing complications. Patients who quickly repay that oxygen debt go on to survive without complications. The longer that it takes to repay that oxygen debt, you either have comorbidities or you go on to become a nonsurvivor. That general window for the payback period to move on without any complications was about 8 hours. If not, cellular dysfunction and death would occur. GDP concepts are founded on two important publications by Ranucci (3) and de Somer (4). Bob (Groom) did a very good review of those two critical papers. Ranucci s and Filip (de Somer) s work confirmed a relationship between low oxygen delivery on CPB and AKI. As oxygen delivery drops below a 270 (Ranucci) or 262 (de Somer) ml O 2 /min/m 2 window, there is an increase in AKI rates. There s also an equally important paper from Dr. Ranucci that we need to add to our repertoire about GDP, and that is his paper on anaerobic metabolism during CPB and the predictive value of carbon dioxide-derived parameters (5). Ranucci demonstrated in this paper the important relationship between the DO 2 i/vco 2 i ratio and lactate production. As the DO 2 i/vco 2 i ratio drops below approximately 5, there is an increase in lactate production. We know that lactate is an important monitoring tool, but there are some problems with lactate monitoring stemming from the delay between when anoxic injury occurs and the time we see serum lactates appear in the bloodstream. These respiratory components of CO 2 production and O 2 delivery are more responsive and are a more immediate measure of predicted lactate production. The work of de Somer confirmed the importance of the DO 2 i/vco 2 i ratio, in their study, the rate of AKI increased significantly as the DO 2 i/vco 2 i ratio dropped below 5.3 (4). Ranucci also illustrated the importance of the respiratory quotient or the CO 2 production index to the oxygen consumption index (5). In normal physiology, a respiratory quotient of.8 1 is normal. As we increase this respiratory quotient and go above 1, we find a corresponding increase in lactate production. The respiratory quotient may also give us some insight into microcapillary perfusion. In an anaerobic state, we are still continuing to produce CO 2, but our oxygen utilization is zero. Increasing anaerobic metabolism yields a higher respiratory quotient or a VCO 2 i/vo 2 i ratio (6). This is an important tool for us in GDP to help us manage distribution of blood flow and possibly recruit microcapillary perfusion. We know that AKI is not all about oxygen delivery, it can be multifaceted and it can come from many sources. Critical O 2 delivery is an important driver in AKI development and long-term survival. Even small amounts of AKI can have significant impact, not only economic but also in patient outcome. A study by Elmistekaway published in 2014 included 3,869 open heart patients and looked at AKI, stage 1 (7). In this study, the rate of AKI, stage 1, was 22.4%. At our institution, when we started GDP, our rate of all type AKI was 25%. AKI can be affected by multiple factors. Even small, stage 1 AKI affects mortality. Elmistekaway demonstrated that patients with stage 1 AKI have a 2.5 times higher mortality rate. They also require longer ventilation, increased length of stay, and have more neurological dysfunction (7). Pickering published a meta-analysis of AKI and CPB in 2015 (8). It includes 46 studies and over 242,000 patients. This analysis showed a CPB-associated AKI rate of 18.1%. Regardless of the scoring method used, the AKIN scoring method, the RIFLE method, or a selfdefined method of AKI, the risk of early mortality from CPB-associated AKI is 4 times greater ( p <.001). In addition, they also demonstrated that the relative risk of stroke associated with AKI from bypass and myocardial infarction was increased (stroke RR = 2.2, myocardial infarction RR = 1.7). So let s talk about time. How much time do we have to respond to critical values and what s the patient outcome? There are a couple of correlates in physiology that you can find which demonstrate a time dose response. A study by Walsh from the Cleveland Clinic included 33,330
3 IS TIMING EVERYTHING? P15 noncardiac surgery patients (9). The goal was to define a true definition of hypotension. This paper demonstrated a time dose relationship between a sustained mean arterial pressure (MAP) less than 55 mm Hg and increased rates of AKI, cardiac complications and myocardial injury. Twenty minutes of pressure less than 55 mm Hg was associated with a 1 1/2 times increase in the rate of AKI. So there re some good correlations with pressure. Walsh also illustrated the relationship of sustained MAP isobars over time. The propensity for AKI and myocardial complications increases dramatically with a MAP less than 55 mm Hg. This time dose relationship is diminished with sustained pressures greater than 60 mm Hg. In a paper published in the Annals of Thoracic Surgery in 2015, Magruder looked at the combined effect of low mean arterial pressure and low oxygen delivery on CPB and AKI rates (10). Their findings demonstrated that if a patient has a mean arterial pressure less than 60 mm Hg for more than 15 minutes during postoperative day zero or one (odds ratio [OR] = 3.96, 95% confidence interval [CI] = , p =.01), or a low oxygen delivery less than 225 ml O 2 /min/m 2 during CPB (OR = 2.46, 95% CI = , p <.001),therewasasignificantly greater odds ratio of developing AKI. In August 2015 in the Clinical Journal of the American Society of Nephrology Raimundo et al. looked at how quickly stage 1 AKI can progress to stage 3 in the setting of low mean arterial pressure and low oxygen delivery (11). If the mean arterial pressure decreased below 65 mm Hg or the oxygen delivery dropped below 300 ml O 2 /min/m 2 in the first12 hours, the patient was more likely to progress to stage 3 AKI ( p =.03). This demonstrates that there is some urgency, not only in treating AKI stage 1, but also in preventing it from happening in the first place. If we look at other physiological systems and their correlation to a time dose response, there are certainly some good references. In 2004, a paper from Yao looked at the area under the curve (AUC) of cerebral oxygen saturations and showed that if you have an AUC less than 40% for more than 10 minutes, you were more likely to suffer from a neurocognitive defect (12). Koning et al. (13,14) present some very interesting work on perfused microcapillary density during CPB. Their data show that not only is there a hemodilution effect but also a nonpulsatile perfusion component to decreased microcapillary density during CPB. At the onset of bypass, there is an immediate decrease in the number of perfused capillaries along with an increase in the velocity of blood flow in through those capillaries. The net result is a significant decrease in the calculated oxygen consumption compared to matched cohorts of off bypass coronary artery bypass graft (CABG) patients (15). This reduced oxygen consumption measured during CPB is due not only to the reduced number of perfused capillaries but also the reduced time for gas exchange due to the increased velocity of blood. This phenomena can last for up to 72 hours postbypass. In terms of GDP values, this is expressed as an increased VCO 2 i/vo 2 i ratio and a markedly reduced VO 2 i, which we often observe during mild hypothermia. GDP may be an important tool in explaining strategies to improve microcirculation during CPB and warrants further investigation. Figure 1 defines the elements of a retrospective review of prospectively collected GDP data for the evaluation of the time dose effect of low oxygen delivery on AKI at the University of Colorado Hospital in This study was composed of 215 CPB patients in whom we calculated a cumulative oxygen debt or oxygen surplus based on a threshold value of 270 ml O 2 /min/m 2. The AUC calculation was the difference between the actual oxygen delivery index relative to 270 multiplied by duration in minutes. We compared that to the absolute nadir and average oxygen delivery as well as the oxygen delivery/carbon dioxide production ratio. A subgroup analysis was adjusted for patients that had preoperative renal failure as defined by a creatinine clearance less than 85 ml/min and did not require a red blood cell transfusion (PRBC). A separate analysis was performed on patients that did receive a PRBC transfusion on CPB. AKI was defined using the AKI Network (AKIN) score and perfusion parameters were collected using the LivaNova CONNECT electronic data management system (LivaNova, Munich, Germany). The all-stage AKI rate was 10% in this patient population. Table 2 lists the demographics for this population. Significant factors for developing CPB-associated AKI included prolonged CPB time ( p =.05), female gender Figure 1. Scatter plot of the AUC analysis showing the cumulative net oxygen delivery on the y axis compared to the peak percentage of baseline creatinine. Orange plots are patients that did not acquire an AKIN-defined kidney injury. Blue plots are patients with a defined AKI. AUC, no-aki patients; RF AUC, patients with any stage AKI.
4 P16 G. JUSTISON Table 2. Demographics of patients included in the time below critical oxygen delivery threshold analysis. No AKI (n = 196) AKI (n = 19) p CPB time (minutes) 142 (79) 214 (73).05 BSA (m 2 ) 2.0 (0.3) 1.9 (0.2).47 BMI (kg/m 2 ) 28 (5.9) 26.6 (5.3).33 % Female Euroscore II 6.1 (10.3) 9.5 (8.5).29 Base OR Hgb (g/dl) 12 (1.9) 10.5 (2.5).04 First CPB Hgb (g/dl) 9.9 (1.7) 9.3 (1.9).27 Nadir Hgb (g/dl) 9.3 (1.7) 8.5 (1.8).13 Last Hgb (g/dl) 9.8 (1.7) 9.4 (1.8).41 Base OR Hgb, first hemoglobin on admission to the operating room; first CPB Hgb, first hemoglobin on bypass; nadir Hgb, lowest hemoglobin on bypass; last Hgb, last hemoglobin on bypass. Values are mean ± 1 SD. ( p =.05), and preoperative anemia ( p =.04). Preoperative risk as calculated by the Euroscore II was not a significant factor (16). All cases were included in this analysis with the exception of transplants and deep hypothermic circulatory arrest procedures. The analysis includes procedures using moderate hypothermia at 28 C. Figure 1 is a scatter plot of all patients in this series. Orange bubbles represent patients that did not develop AKI. Blue bubbles are patients that did develop AKI, stage 1 or greater. The x axis represents the peak postoperative creatinine value as a percentage of the baseline preoperative value. Moving along this scale from left to right on the x axis represents an increasing level or severity of AKI. The y axis represents the cumulative oxygen debt or surplus based on our defined AUC calculation. Positive values represent a cumulative oxygen surplus for the duration of CPB and a negative value represents a net oxygen debt over the duration of CPB. Table 3 represents the GDP values for patients that did and did not develop AKI. When we look at these two groups, we see that patients that developed AKI had a lower average nadir oxygen delivery on CPB (243 vs. 297 ml O 2 /min/m 2, p <.001). Patients with CPB-associated AKI spent more cumulative time (minutes) below the 270 ml O 2 /min/m 2 threshold (33 vs. 14 minutes in the no-aki group, p =.01), and of course had a higher average Table 3. GDP profile of patients who develop AKI. No AKI (n = 196) AKI (n = 19) p Average nadir DO 2 i (ml O 2 /min/m 2 ) 297 (54.5) 243 (16.9) <.001 Average TB 270 ml O 2 /min/m 2 (min) 14 (3.4) 33 (23.3).01 % Base Cr (mg/dl) 103 (26.6) 185 (36.8) <.001 AUC (ml O 2 /m 2 ) 386 (7.9) 779 (144).01 Nadir DO 2 i/vco 2 i ratio 5.5 (.1) 4.2 (1.6).002 Average TB 270 is the average time in minutes spent below the critical oxygen delivery of 270 ml O 2 /min/m 2. Values are mean ± 1 SD. increase in creatinine. The group that developed AKI had a net cumulative oxygen debt compared to the group which did not acquire CPB-associated AKI. The other critical observation was that patients who developed AKI had a nadir DO 2 i/vco 2 i ratio less than 5 indicating that perhaps the oxygen delivery as a global measure was insufficient for those patients (no-aki 5.5 vs. AKI 4.2, p =.002). These findings are consistent with the work reported by de Somer, which first made this relationship between the DO 2 i/vco 2 i ratio and AKI (4). As a subset analysis, we adjusted out patients who had preoperative renal insufficiency, defined as a preoperative creatinine clearance less than 85 ml/min calculated using the Cockroft Gault creatinine clearance calculator (16). The rate of all type CPB-associated AKI in this group is 8.2% (Table 4). In this scenario, we find a significant factor again is length of bypass time ( p =.03). Neither the hemoglobin profile on bypass nor the average mean arterial pressures are factors in developing AKI in this patient cohort. Neither was the average nadir or mean DO 2 i significant between the two groups. The average nadir DO 2 i in theno-akigroupwas296mlo 2 /min/m 2 compared to 286 ml O 2 /min/m 2 in the AKI group ( p =.70). This was above the selected reference threshold of 270 ml O 2 /min/m 2. In the AKI group, there were more minutes during the bypass run where we fell below 270 ml O 2 / min/m 2 (no-aki 16.1 minutes vs. AKI 37.3 minutes, p =.03). The most significant GDP parameter between the two groups was again the DO 2 i/vco 2 i ratio. The average nadir DO 2 i/vco 2 i ratio in the AKI group was 4.2 compared to 5.5 in the no-aki group ( p <.001), indicating that globally oxygen delivery may be insufficient for those patients current metabolic demands as reflected by the DO 2 i/vco 2 i ratio. Longer bypass times allow you more opportunities to fall below that critical threshold and demonstrate the importance of continuous GDP monitoring. Having the complete respiratory picture, including Table 4. Comparison of GDP values for both patient groups adjusted for preoperative renal failure. No AKI (n = 170) AKI (n = 14) p % Baseline creatinine (mg/dl) <.001 CPB time (minutes) Baseline hemoglobin (g/dl) First CPB hemoglobin (g/dl) Nadir hemoglobin (g/dl) Last hemoglobin (g/dl) % Time SvO 2 > 65% Nadir DO 2 i (ml O 2 /min/m 2 ) Mean DO 2 i (ml O 2 /min/m 2 ) Time below DO 2 i = 270 (minutes) Nadir DO 2 i/vco 2 i <.001 Values are mean ± 1 SD.
5 IS TIMING EVERYTHING? P17 this DO 2 i/vco 2 i ratio, was more predictive of AKI than the DO 2 i alone in this patient cohort. The value of the DO 2 i/vco 2 i ratio becomes even more apparent when you look at patients that require a transfusion or patients who are operating in an anemic state (Table 5). In this group bypass, time was not a significant factor. The all type CPB-associated AKI rate in this subset was 19%. The nadir and mean oxygen delivery was similar in both patients that did and did not develop AKI. In both groups, the average nadir DO 2 i was less than the 270 threshold (240 ml O 2 /min/m 2 in the no-aki group vs. 248 ml O 2 /min/m 2 in the AKI group, p =.44). Although the AKI group spent more minutes below the 270 ml O 2 /min/m 2 threshold, it was not significant. The factor that was predictive of AKI was again the DO 2 i/ VCO 2 i ratio. The DO 2 i/vco 2 i ratio in the no-aki group was 4.8 compared to 3.9 in the patients who went on to develop CPB-associated AKI ( p <.001). This illustrates that each patient will dictate what their own DO 2 critical threshold is and the DO 2 i/vco 2 i ratio will confirm if that oxygen delivery index is appropriate. The volume of PRBC transfusion was not different in this subset but the time to intervention (time it took the perfusionist to increase the DO 2 i) was. In the group that developed AKI, it took an average of 37 minutes to respond to a low DO 2 i compared to 16 minutes in the no-aki group ( p =.03). If we go back to Figure 1 and look at patients that did and did not develop AKI, you can see some both above and below this relative oxygen debt or oxygen surplus line along the y axis. So we must ask the question, why do some patients who have an average oxygen delivery greater than 270 ml O 2 /min/m 2 (defined oxygen surplus) go on to develop AKI, and why are some patients who have an average oxygen delivery less than 270 ml O 2 /min/m 2 (defined oxygen debt) not developing AKI? Table 5. Comparison of time below threshold data in patients that develop AKI vs. no AKI and received a red blood cell transfusion on CPB. No AKI (n = 26) AKI (n =5) p % Baseline Creatinine (mg/dl) <.001 CPB time (minutes) BSA (m 2 ) BMI (kg/m 2 ) Euroscore II % Female <.001 Baseline hemoglobin (g/dl) MAP (mm Hg) Nadir DO 2 i (ml O 2 /min/m 2 ) Mean DO 2 i (ml O 2 /min/m 2 ) Time below DO 2 i = 270 (minutes) Nadir DO 2 i/vco 2 i <.001 % time SvO 2 > 65% Time to first intervention (minutes) Mean PRBC units What we find is that even though the DO 2 i was greater than 270 ml O 2 /min/m 2,aratiolessthan5waspredictive of AKI. Patients can have an oxygen delivery less than 270 ml O 2 /min/m 2 as long as that DO 2 i/vco 2 i ratio remains over 5 (Table 6). In the patients with an average nadir less than threshold, the mean was 264 ml O 2 /min/m 2 but the DO 2 i/vco 2 i ratiowas5.7,whichwas above the 5.3 threshold suggested by de Somer. A retrospective analysis by Bennett et al. (17) presented an interesting conclusion in regards to oxygen delivery and AKI. They were comparing a minimal bypass circuit to a conventional bypass circuit. They found in the minimal bypass circuit group, the average cardiac index was less than in a conventional bypass circuit, but the reduced hemodilution in the mini-bypass circuits resulted in a higher hemoglobin than their conventional circuits. The net result was oxygen delivery between their two circuits was relatively the same. They concluded the risk of developing AKI increased by 1% for every 1 O 2 /min/m 2 decrease in oxygen delivery. So that leads us to clinical trials. Currently, there is a multicenter, international, randomized prospective trial called the GIFT trial or Goal directed perfusion Trial, which is investigating GDP management strategies vs. a body surface area indexed bypass flow management. The control group is a conventional 2.4 cardiac index management strategy compared to the study patients, which manage hemoglobin flow to maintain oxygen delivery greater than 280 and compare these CPB management strategies effect on new AKI. We anticipate results from this study in early In conclusion, there is a time dose relationship between low oxygen delivery and AKI. The global marker of adequate oxygen delivery, the DO 2 i/vco 2 i ratio, is more predictive than oxygen delivery alone. And as we study GDP more, we re learning that there is really increased value, in understanding the respiratory quotient and its relationship to patient outcomes. Determinants of low oxygen delivery, mainly blood flow and hemoglobin, should be corrected quickly. Thank you again for your attention. I hope you find this session to be informative and take some of these back to your practice. Table 6. GDP characteristics of patients that had a positive AUC (net oxygen surplus) and developed AKI compared to those with a negative AUC (net oxygen deficit) and did not develop AKI. GDP characteristic +AUC DO 2 i > and AKI AUC DO2i < 270 and no AKI AUC (ml O 2 /m 2 ) Nadir DO 2 i (ml O 2 /min/m 2 ) Nadir DO 2 i/vco 2 i
6 P18 G. JUSTISON REFERENCES 1. Galletti PM, Brecher GA. Heart-Lung Bypass, Principles and Techniques of Extracorporeal Circulation. New York, NY: Grune & Stratton; 1962: Shoemaker WC, Appel PL, Kram HB. Role of oxygen debt in the development of organ failure sepsis, and death in high-risk surgical patients. Chest. 1992;102: Ranucci M, Romitti F, Isgro G, et al. Oxygen delivery during cardiopulmonary bypass and acute renal failure after coronary operations. Ann Thorac Surg. 2005;80: de Somer F, Mullholland J, Bryan M, Alosio T, Van Nooten G, Ranucci M. O 2 delivery and CO 2 production during cardiopulmonary bypass as determinants of acute kidney injury: Time for a goal-directed perfusion management? Crit Care. 2011;15:R Ranucci M, Isgro G, Romitti F, et al. Anaerobic metabolism during cardiopulmonary bypass: Predictive value of carbon dioxide derived parameters. Ann Thorac Surg. 2006;81: Ranucci M, Carboni G, Cotza M. de cardiopulmonary bypass: Pathophysiology, measure and clinical relevance. Perfusion. 2017;32: Elmistekaway E, McDonald B, Hudson C, et al. Clinical impact of mild acute kidney injury after cardiac surgery. Ann Thorac Surg. 2014;98: Pickering JW, James MT, Palmer SC. Acute kidney injury and prognosis after cardiopulmonary bypass: A meta-analysis of cohort studies. Am J Kidney Dis. 2015;65: Walsh M, Devereaux PJ, Garg AX, et al. Relationship between mean arterial pressure and clinical outcomes after noncardiac surgery: Toward and empirical definition of hypotension. Anesthesiology. 2013;119: Magruder JT, Dungan SP, Grimm JC, et al. Nadir oxygen delivery on bypass and hypotension increase acute kidney injury after cardiac operations. Ann Thorac Surg. 2015;100: Raimundo M, Crichton S, Syed Y, et al. Low systemic oxygen delivery and BP and risk of progression of early AKI. Clin J Am Soc Nephrol. 2015;10: YaoF,TsengCA,HoCA,LevinSK,IllnerP.Cerebraloxygen desaturation is associated with early postoperative neuropsychological dysfunction in patients undergoing cardiac surgery. J Cardiothorac Vasc Anesth. 2004;18: Koning NJ, de Lange F, Vonk AB, et al. Impaired microcirculatory perfusion in a rat model of cardiopulmonary bypass: The role of hemodilution. Am J Physiol Heart Circ Physiol. 2016;310: H Koning NJ, Simon LE, Asfar P, Baufreton C, Boer C. Systemic microvascular shunting through hyperdynamic capillaries after acute physiological disturbances following cardiopulmonary bypass. Am J Physiol Heart Circ Physiol. 2014;307:H Koning NJ, Vonk AB, Meesters MI, et al. Microcirculatory perfusion is preserved during off-pump but not on-pump cardiac surgery. J Cardiothorac Vasc Anesth. 2014;28: Roques F, Michel P, Goldstone AR, Nashef SA. The logistic EuroSCORE. Eur Heart J. 2003;24: Bennett MJ, Rajakaruna C, Bazerbashi S, Webb G, Gomez-Cano M, Lloyd C. Oxygen delivery during cardiopulmonary bypass (and renal outcome) using two systems of extracorporeal circulation: A retrospective review. Interact Cardiovasc Thorac Surg. 2013;16:760 4.
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