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Ann Thorac Surg 2003;76:784-791
© 2003 The Society of Thoracic Surgeons
a Department of Anesthesiology, Duke University Medical Center, Durham, North Carolina, USA
b Department of Medicine, Duke University Medical Center, Durham, North Carolina, USA
c Department of Surgery, Duke University Medical Center, Durham, North Carolina, USA
Accepted for publication March 13, 2003.
* Address reprint requests to Dr Stafford-Smith, Department of Anesthesiology, Box 3094, Duke University Medical Center, Durham, NC 27710, USA;
e-mail: staff002{at}mc.duke.edu
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Abstract |
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METHODS: Demographic, perioperative, and laboratory data were gathered for 1,404 primary elective coronary bypass surgery patients. Preoperative and daily postoperative creatinine values were measured until hospital discharge per institutional protocol. Stepwise multivariable linear regression analysis was performed to determine whether lowest hematocrit during CPB was independently associated with peak fractional change in creatinine (defined as the difference between the preoperative and peak postoperative creatinine represented as a percentage of the preoperative value). A p value of less than 0.05 was considered significant.
RESULTS: Multivariable analyses including preoperative hematocrit and other perioperative variables revealed that lowest hematocrit during CPB demonstrated a significant interaction with body weight and was highly associated with peak fractional change in serum creatinine (parameter estimate [PE] = 4.5; p = 0.008) and also with highest postoperative creatinine value (PE = 0.06; p = 0.004). Although other renal risk factors were significant covariates in both models, TM50 (an index of hypotension during CPB) was notably absent.
CONCLUSIONS: These results add to concerns that current CPB management guidelines accepting extreme hemodilution may contribute to postoperative acute renal and other organ injury after cardiac surgery.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsReferences |
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The rationale for the renoprotective effect of hemodilution involves reduction of blood viscosity and improved regional blood flow in the setting of hypoperfusion and hypothermia [8, 9]. However several recent papers have reported independent associations of lowest hematocrit during CPB with morbidity and mortality after cardiac surgery [10–12]. In this regard the cutoff for "safe" hemodilution has yet to be defined. Various "minimum acceptable" hematocrit values have been proposed based on animal experiments ranging from 9% to 18% [13, 14]. The relationship between current extreme hemodilution strategies and renal injury after cardiac surgery has not yet been investigated. Therefore we tested the hypothesis that lowest hematocrit during CPB is independently associated with acute renal injury after cardiac surgery.
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Patients and methods |
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Renal function assessment
Serum creatinine was measured as part of routine biochemical laboratory investigations for all elective coronary bypass surgery patients using a dry slide enzymatic reflectance technique (VITROS 950; Johnson and Johnson, New Brunswick, NJ) with a normal range of 0.7 to 1.4 mg/dL (62 to 124 µmol/L).
Definition of variables
The preoperative serum creatinine (CrPre) was identified as the value on the day before surgery for all inpatients, and was assessed within 1 week prior to surgery for all outpatients scheduled to undergo elective coronary artery bypass graft surgery. Peak postoperative creatinine (CrmaxPost) was defined as the highest of the daily in-hospital postoperative values. Peak percentage change in postoperative creatinine (%
Cr) was defined as the difference between the CrPre and CrmaxPost represented as a percentage of the preoperative value. Using the Cockroft Gault equation [16] preoperative creatinine clearance (CrClPre) was estimated from CrPre and lowest postoperative creatinine clearance (CrClPost) was estimated from CrmaxPost.
The primary outcome variable, %Cr, was selected as the marker that demonstrates the best association with mortality and major morbidity after coronary bypass surgery when compared other creatinine-derived markers of renal function [17], a consistent finding, regardless of preoperative renal status, that persists even in separate analysis of the group of patients who serum creatinine values never exceed the normal range. In our previous work we noted %Cr after coronary bypass surgery to be remarkably similar among patient groups that differ by baseline renal function, creatinine values simply assuming proportionate but different absolute changes. CrmaxPost and lowest postoperative creatinine clearance were selected as secondary outcomes for analysis as they also highly correlate with postoperative morbidity and mortality but closely reflect impairment of renal filtration function [17].
Hematocrit, hemodynamic, and transfusion data
Hematocrit was measured every 15 minutes during CPB as part of routine arterial blood gas analysis protocols using the AVL Omni Modular System blood gas analyzer (Roche Diagnostics, Indianapolis, IN). Hemodynamic parameters were available for each minute during CPB from the ARKIVE Information Management System (Arkive IMS, San Diego, CA). The TM50 is a previously reported, derived index of the degree and duration of low CPB perfusion pressure [18, 19]. The TM50 was defined as the time-pressure integral mean CPB blood pressure less than 50 mm Hg (minmm Hg) or as the area under the CPB blood pressure curve below 50 mm Hg. Transfusion was defined in two variables: (1) RBC 48 hours: the number of units of packed red cells given within the first 48 hours postoperatively; and (2) transfusion: transfusion of more than 2 units of packed red cells and at least one other blood product.
Anesthesia and surgery
Anesthesia was managed per the attending anesthesiologist’s preference. Use of agents with potential renal effects (eg, intravenous dopamine, diuretics, antifibrinolytic agents) were not controlled. Extracorporeal perfusion was performed using a Cobe CML Duo blood oxygenator with sealed hard-shell filtered venous reservoir (Cobe Laboratories, Lakewood, CO), a Cobe Century Perfusion System (Cobe Laboratories), and a 43-micron arterial line filter (Cobe Sentry arterial line filter with Primegard; Cobe Cardiovascular, Arvada, CO). Blood obtained by cardiotomy suction was routed by the roller pump into the integrated oxygenator-venous reservoir. Nonpulsatile perfusion was maintained at 2 to 2.4 L · min-1 · m-2. The target CPB perfusion rate of 2 to 2.4 L · min-1 · m-2 was maintained throughout the weight range. Other standard perfusion guidelines included titration of CPB perfusion rate to maintain a SvO2 of at least 60% during normothermic and 70% during hypothermic CPB.
The bypass circuit was primed with mannitol (50 g of 20% solution) and crystalloid solution (0.9% normal saline). Typically, acceptable hematocrit ranged from 22% to 24% during bypass, with red blood cell transfusion usually occurring when values below 20% were observed. The arterial carbon dioxide tension was maintained throughout bypass at 35 to 40 mm Hg (uncorrected for temperature) with the arterial oxygen tension maintained at 150 to 250 mm Hg. Target mean arterial pressure was between 50 and 70 mm Hg during bypass using intravenous phenylephrine or sodium nitroprusside as required. Typically patients were cooled to a nasopharyngeal temperature of 34°C to 28°C during bypass and rewarmed to a nasopharyngeal temperature of 37°C or a bladder temperature of at least 36°C prior to separation from bypass.
Statistical analysis
Simple descriptive statistics (mean, standard deviation) were used to describe the population demographics.
We performed a primary stepwise multivariable linear regression analysis to test the association of lowest hematocrit during bypass with %Cr. To assess robustness of the results and to increase generalizability, secondary multivariable regression analyses were also performed to test the association between lowest hematocrit during bypass and CrmaxPost and CrClPost. First we performed a full-model analysis in which we included all the demographic, comorbidity, and intraoperative data. To follow up this analysis we implemented a stepwise selection so that the final model included only variables that were significantly associated with (p < 0.10) the outcome (%Cr). Of note the secondary analysis using CrmaxPost, while controlling for preoperative creatinine, is closely equivalent (and statistically identical) to assessing pre to peak change (ie, delta) in creatinine. All statistical analyses were performed using the SAS Statistical software (software version 8.0; SAS Institute, Cary, NC). A p value of less than 0.05 was considered significant.
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Cr (Table 3),
we found a significant two-way interaction between body weight and lowest hematocrit during bypass (parameter estimate [PE] = -0.05; p = 0.007). With the inclusion of the hematocrit-body weight interaction in this model, there was a highly significant association between lowest hematocrit during bypass and %Cr (PE = 4.5; p = 0.008). Figure 1 shows the influence of body weight on the association between lowest hematocrit during bypass and %Cr. Other variables known to be renal risk factors including preoperative creatinine (CrPre), body weight, Charlson comorbidity score, prebypass serum glucose, perioperative blood transfusion, preoperative hematocrit, and postoperative IABP and inotrope use were also significantly associated with %Cr in this multivariable model (Table 3). It is noteworthy that the association between lowest hematocrit during bypass and %Cr was significant even after accounting for preoperative hematocrit. Figure 2
demonstrates the relationship of lowest hematocrit during bypass to %Cr in patients weighing 75 kg or more, with 95% confidence limits. To address the question of whether there is an "elbow" in the data where the slope of the relationship between lowest hematocrit during bypass and %Cr changes significantly, we used a restricted cubic splines analysis of our regression model. We found no significant cutoff where the association between lowest hematocrit during bypass and %Cr diverged from a linear relationship.
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Cr (p = 0.0008, beta coefficient = 9.8). Because the predictors are related to each other and also to the outcome, this raises the issue of confounding that cannot be completely addressed by our statistical models. However because the inclusion of inotropes in the multivariable model (see Table 3) does not alter the significance of our predictors of interest (weight, lowest hematocrit during bypass, and the interaction term) we conclude that these variables contribute an independent predictive ability beyond the role of postoperative inotropes. A second concern in interpretation of our data relates to the issue of transfusion and lowest hematocrit during bypass because it is difficult to separate the effects of transfusion from the need for transfusion as they would always be expected to occur together—that is, everyone who needs a transfusion gets a transfusion. We found an association between lower hematocrits during bypass and increased transfusion in a univariate regression model (p < 0.0001, beta coefficient = -0.07). However because the inclusion of red blood cells transfusion in the model does not alter the significance of our predictors we again conclude that these variables contribute independent predictive ability. Because this relationship raises the issue of interdependent variables we performed tolerance and variance inflation diagnostics on our models designed to detect the presence of multicollinearity. When lowest hematocrit during bypass and transfusion are in a model together, the tolerance for the variables is 0.78 and 0.92 respectively (corresponding to variance inflation values of 1.3 and 1.1). Because the tolerance values are greater than 0.4 we conclude that the model is appropriate statistically. Using correlated variables as predictors in a model requires careful consideration and careful interpretation our diagnostics indicate that our models do not violate accepted guidelines for multicollinearity.
Because hematocrit is directly influenced by concurrent blood transfusion we performed a subsequent analysis of the relationship between perioperative transfusion, lowest hematocrit during bypass, and %Cr (see Fig 4).
For any given lowest hematocrit during bypass we found a direct relationship between increased transfusion and greater %Cr.
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Comment |
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Cr and CrmaxPost. We also confirmed associations of previously recognized renal risk factors [3, 4] including elevated preoperative creatinine, Charlson comorbidity index, intraoperative highest prebypass serum glucose, postoperative inotrope and IABP use, preoperative hematocrit, blood transfusion and body weight with both, %Cr and CrmaxPost. The absence of low bypass perfusion pressure (TM50) as a significant factor in both multivariable analyses is notable and confirms previous reports of lack of evidence of perfusion pressure as a predictor of renal dysfunction [20–22]. The study design, large number of patients, and the use of valid markers of renal injury are the strengths of this study. The significant association of lowest hematocrit during bypass with both creatinine markers is consistent with an important contributory role of hemodilution in the pathophysiology of acute perioperative renal injury after cardiac surgery. The effects of hemodilution during bypass on various organ systems are well described [14, 23, 24]. The range of lowest hematocrit during bypass in our study was almost identical to that observed in the two major previous publications relating hemodilution during bypass with postoperative complications involving 9,700 patients (10% to 33% versus 10% to 36% and 10% to >35%) [10, 11]. In addition our mean lowest hematocrit during bypass (19.5%) was similar to those quoted in these studies, including one center reporting 2,738 patients with a mean lowest hematocrit of 18.8% [11]. Hemodilution reduces the need for addition of blood to the bypass circuit, both avoiding transfusion and reducing viscosity during hypothermic bypass. As acid-base abnormalities do not develop routinely during bypass, the resultant increase in regional blood flow during bypass has been thought to compensate for the reduced oxygen carrying capacity of the perfusate compared with prebypass levels. However the breakdown of the balance between oxygen supply and demand in this setting has not otherwise been extensively studied. Although the association of hemodilution or low hematocrit with adverse outcomes after cardiac surgery has been reported [10–12] the degree of hemodilution that can be tolerated before an adverse effect occurs is not yet known. DeFoe and colleagues [10] reported an unfavorable association between lowest hematocrit during bypass and adverse in-hospital outcomes after cardiac surgery in a large group of patients in an observational study. However this study did not comment on adverse renal outcomes and did not investigate perioperative renal dysfunction as a primary outcome. In another retrospective analysis, Fang and coworkers [11] reported that lowest hematocrit during bypass was independently associated with mortality after cardiac surgery. This study also recognized preoperative renal failure as one of the risk factors for mortality in addition to lowest hematocrit but did not identify perioperative renal dysfunction as an adverse outcome related to lowest hematocrit during bypass. Ranucci and associates [12] found a hematocrit of less than 25% during bypass, low output syndrome, and homologous blood transfusions to be predictors of severe renal dysfunction in 316 patients undergoing cardiac surgery. However the results from this study were based on a regression analysis looking at three outcome variables in a subgroup of only 9 patients with severe renal dysfunction. These results also did not correct for preoperative creatinine, which is known to influence postoperative creatinine rise [3]. Our study investigates the independent association of lowest hematocrit during bypass with acute renal injury as a primary outcome in coronary bypass surgery patients.
Our report has limitations related to study design and measurement of renal function. Although this study is retrospective, the data were taken from a prospectively gathered quality-assurance database. A second concern is that our study evaluated only one aspect of renal function, namely filtration, and not other renal homeostatic roles including osmolality, electrolyte and acid-base regulation and production, and release of enzymes and hormones. Although more sensitive markers of subtle renal injury than creatinine such as urinary N-acetyl ß-D-glucosaminidase [25] and cystatin C [26] have been reported, the link between these markers and adverse postoperative complications has not been established [27]. Moreover creatinine-based markers have consistently proved to be both sensitive indicators of renal injury and robust prognostic indicators of adverse outcome in patients with cardiovascular disease [28, 29] including those undergoing cardiac surgery [30]. We found a significant association between blood transfusion and acute renal injury. A potential concern is that extreme hemodilution may simply be a marker for increased likelihood of blood transfusion. Supporting this interpretation is the interaction we observed between hemodilution, body weight, and renal injury, with greater transfusion requirements to achieve a "target hematocrit" in an overweight patient. However in our multivariable analyses accounting for blood transfusion we still found lowest hematocrit during bypass to be significantly associated with postoperative creatinine rise (Tables 3, 4; Figs 1–3). Despite these limitations we feel that the use of valid markers of renal injury combined with data analysis in a large group of patients strengthen the significance of our findings.
Although cause and effect are not demonstrated by our findings of an association of severe hemodilution during bypass and acute renal injury, it is important to explore possible physiologic foundations for this relationship. Because hematocrit is directly related to tissue oxygen delivery a simple interpretation of our findings is that severe hemodilution may contribute to renal injury by augmenting the local renal inflammatory response as a result of ischemia-reperfusion injury, particularly in the hypoxic environment of the renal medulla. However hemodilution has previously been thought to be renoprotective [31]. In an animal model of ischemic acute renal injury, Olof and colleagues [32] reported that trapping of red blood cells in the medullary vasculature and associated reductions in outer medullary blood flow observed with normal and elevated hematocrits are completely avoided with hemodilution (30%). Although other authors confirmed the avoidance "red cell trapping" with hemodilution, they could not confirm a benefit in terms of reduced renal injury [33, 34].
In a randomized study of 300 patients we did not find a difference between warm and cold bypass, with regard to renal injury, [7], suggesting a pathophysiology independent of oxygen demand. Other factors than ischemia-reperfusion injury such as atheroembolism and systemic inflammatory response have been implicated as important contributors to post–cardiac surgery nephropathy. Koh and colleagues [35] speculated that alterations in the pattern of aortic blood flow related to cardiopulmonary bypass, potentially including the effects of hemodilution, may increase emboli delivery to the kidney and other organs. The relationship of hemodilution and inflammation during bypass is not known but it is possible that gut ischemia related to reduced tissue oxygen delivery may result in greater release of endotoxin and inflammation- mediated renal injury [36]. Visceral fat is a key regulator site for the process of inflammation and obesity is associated with an upregulated inflammatory state [37]. The interaction between lowest hematocrit during bypass and increased weight that we observed in our study may be explained by the combining of effects that increase inflammatory stimuli and inflammatory response respectively.
The significant association between lowest hematocrit during bypass and acute renal injury raises concerns regarding currently accepted bypass management strategies. Current guidelines for accepted levels of hemodilution during bypass do not lead to the development of acid-base disturbances. However occult cellular hypoxemia and injury may still occur. Such injury in the renal medulla, a tissue that is known to have a precarious balance between oxygen supply and demand even under normal conditions [38], may be the basis of the findings of our study. Strategies to avoid extreme hemodilution may include transfusion. However since transfusion of red cells is also independently associated with creatinine rise in our study (see Tables 3, 4; Fig 4) guidelines for optimal hematocrit during bypass that include transfusion cannot be simply defined. The decision to transfuse is usually based on clinical judgment, institutional protocols, and hematocrit "triggers." Because transfusion has not been tested as a primary outcome of this study the authors cannot recommend changes in transfusion policy based on its effect on perioperative creatinine changes. However clearly minimizing bypass prime volumes should reduce anemia without transfusion and potentially reduce renal risk. Our data suggest that hemodilution during bypass should be carefully monitored and excessive falls in hematocrit avoided, especially in overweight patients (see Fig 2). We did not observe an "elbow" in the graph relating lowest hematocrit to %Cr that would suggest a level below which hematocrit is detrimental to renal function.
In summary we found an independent association between lowest hematocrit during bypass and postoperative creatinine rise that is influenced by body weight. This association was significant for all creatinine markers of renal injury that we assessed (%Cr, CrmaxPost, and CrClPost). We did not observe an effect of low bypass perfusion pressure on creatinine rise. This is the first report highlighting the association of extreme hemodilution during bypass with acute renal injury as a primary outcome. Despite being a retrospective data analysis looking at one aspect of renal function we believe that the study design and the use of valid markers of renal injury justify our conclusions. Our findings question the wisdom of tolerating low levels of hematocrit during bypass. We have previously reported the lack of effect of bypass temperature on acute renal injury [7]. These findings suggest that optimal bypass management guidelines should emphasize the maintenance of adequate hematocrit levels during bypass regardless of temperature protocol employed. However the independent contributions of hemodilution and transfusion to the pathophysiology of perioperative renal injury require further examination in a prospective randomized trial looking at a variety of tests of renal function.
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K. G. Shann, D. S. Likosky, J. M. Murkin, R. A. Baker, Y. R. Baribeau, G. R. DeFoe, T. A. Dickinson, T. J. Gardner, H. P. Grocott, G. T. O'Connor, et al. An evidence-based review of the practice of cardiopulmonary bypass in adults: A focus on neurologic injury, glycemic control, hemodilution, and the inflammatory response. J. Thorac. Cardiovasc. Surg., August 1, 2006; 132(2): 283 - 290.e3. [Full Text] [PDF]
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S. D. Surgenor, G. R. DeFoe, M. P. Fillinger, D. S. Likosky, R. C. Groom, C. Clark, R. E. Helm, R. S. Kramer, B. J. Leavitt, J. D. Klemperer, et al. Intraoperative Red Blood Cell Transfusion During Coronary Artery Bypass Graft Surgery Increases the Risk of Postoperative Low-Output Heart Failure Circulation, July 4, 2006; 114(1_suppl): I-43 - I-48. [Abstract] [Full Text] [PDF]
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R. H. Habib, A. Zacharias, T. A. Schwann, C. J. Riordan, S. J. Durham, and A. S. Shah Postoperative Renal Dysfunction After On-Pump Versus Off-Pump Coronary Revascularization: Role of On-Pump Hemodilution and Transfusions Ann. Thorac. Surg., April 1, 2006; 81(4): 1548 - 1549. [Full Text] [PDF]
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 S. Beholz, L. Zheng, M. Rusche, M. Kessler, and W. Konertz Low-Prime System Minimizes Transfusions and Hemodilution in Coronary Bypass Asian Cardiovasc Thorac Ann, February 1, 2006; 14(1): 10 - 13. [Abstract] [Full Text] [PDF]
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M. H. Rosner and M. D. Okusa Acute Kidney Injury Associated with Cardiac Surgery Clin. J. Am. Soc. Nephrol., January 1, 2006; 1(1): 19 - 32. [Abstract] [Full Text] [PDF]
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S. S. F. Fischer, B. Phillips-Bute, M. Swaminathan, C. Milano, and M. Stafford-Smith SymmetryTM Aortic Connector Devices and Acute Renal Injury: A Comparison of Renal Dysfunction After Three Different Aortocoronary Bypass Surgery Techniques Anesth. Analg., January 1, 2006; 102(1): 25 - 31. [Abstract] [Full Text] [PDF]
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M. Ranucci, F. Romitti, G. Isgro, M. Cotza, S. Brozzi, A. Boncilli, and A. Ditta Oxygen Delivery During Cardiopulmonary Bypass and Acute Renal Failure After Coronary Operations Ann. Thorac. Surg., December 1, 2005; 80(6): 2213 - 2220. [Abstract] [Full Text] [PDF]
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J. H. Shuhaiber Randomized prospective trial for blood transfusion during adult cardiopulmonary bypass surgery J. Thorac. Cardiovasc. Surg., May 1, 2005; 129(5): 1200 - 1201. [Full Text] [PDF]
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M. Stafford-Smith Evidence-Based Renal Protection in Cardiac Surgery Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 2005; 9(1): 65 - 76. [Abstract] [PDF]
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K. Karkouti, W.S. Beattie, D.N. Wijeysundera, V. Rao, C. Chan, K.M. Dattilo, G. Djaiani, J. Ivanov, J. Karski, and T.E. David Hemodilution during cardiopulmonary bypass is an independent risk factor for acute renal failure in adult cardiac surgery J. Thorac. Cardiovasc. Surg., February 1, 2005; 129(2): 391 - 400. [Abstract] [Full Text] [PDF]
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B. D. Spiess Transfusion of Blood Products Affects Outcome in Cardiac Surgery Seminars in Cardiothoracic and Vascular Anesthesia, December 1, 2004; 8(4): 267 - 281. [Abstract] [PDF]
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M. Swaminathan, B. G. Phillips-Bute, and M. Stafford-Smith Reply Ann. Thorac. Surg., November 1, 2004; 78(5): 1881 - 1882. [Full Text] [PDF]
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M. Ranucci, L. Menicanti, and A. Frigiola Acute Renal Injury and Lowest Hematocrit During Cardiopulmonary Bypass: Not Only a Matter of Cellular Hypoxemia Ann. Thorac. Surg., November 1, 2004; 78(5): 1880 - 1881. [Full Text] [PDF]
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M. Ranucci, G. Soro, N. Barzaghi, A. Locatelli, G. Giordano, A. Vavassori, A. Manzato, C. Melchiorri, T. Bove, G. Juliano, et al. Fenoldopam Prophylaxis of Postoperative Acute Renal Failure in High-Risk Cardiac Surgery Patients Ann. Thorac. Surg., October 1, 2004; 78(4): 1332 - 1337. [Abstract] [Full Text] [PDF]
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F. Merkle, W. Boettcher, F. Schulz, A. Koster, M. Huebler, and R. Hetzer Perfusion technique for nonhaemic cardiopulmonary bypass prime in neonates and infants under 6 kg body weight Perfusion, July 1, 2004; 19(4): 229 - 237. [Abstract] [PDF]
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 A. Lassnigg, D. Schmidlin, M. Mouhieddine, L. M. Bachmann, W. Druml, P. Bauer, and M. Hiesmayr Minimal Changes of Serum Creatinine Predict Prognosis in Patients after Cardiothoracic Surgery: A Prospective Cohort Study J. Am. Soc. Nephrol., June 1, 2004; 15(6): 1597 - 1605. [Abstract] [Full Text] [PDF]
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P. E. Antunes, D. Prieto, J. F. de Oliveira, and M. J. Antunes Renal dysfunction after myocardial revascularization Eur J Cardiothorac Surg, April 1, 2004; 25(4): 597 - 604. [Abstract] [Full Text] [PDF]
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