Effects of phosphorylcholine coating on extracorporeal circulation management and postoperative outcome: a double-blind randomized study
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1 doi: /icvts Interactive CardioVascular and Thoracic Surgery 8 (009) 7 11 Work in progress report - Cardiopulmonary bypass Effects of phosphorylcholine coating on extracorporeal circulation management and postoperative outcome: a double-blind randomized study a, a a b Roberto Lorusso *, Giuseppe De Cicco, Pasquale Totaro, Sandro Gelsomino a Experimental Cardiac Surgery Unit and Blood Laboratory, Civic Hospital, Piazzale Spedali Civili, 1, 515 Brescia, Italy b Experimental Surgery Unit, Department of Heart and Vessels, Careggi Hospital, Florence, Italy Received 4 January 008; received in revised form 16 July 008; accepted 8 July 008 Abstract The aim of the study was to evaluate the effects of phosphorylcholine coating (PC) on intra-operative extracorporeal circulation (ECC) management and perioperative outcome. One hundred and twenty consecutive cardiac surgery patients were enrolled for the study. Patients were randomly assigned to ECC with PC circuits (60 patients) or to corresponding non-coated circuits (60 patients). Transoxygenator pressure drop, blood flows, flow resistances and ECC parameters were recorded at surgery before ECC institution and every 10 min thereafter until ECC discontinuation. Postoperative variables (hematological parameters, drainage blood loss, mechanical ventilation time, incidence of atrial fibrillation, use of blood products) were also assessed and compared between groups. No differences were found between the two groups in terms of demographics, operative, and hematological profiles. PC showed, at equal pump flows, to significantly (P-0.01) attenuate pressure drop across oxygenators and to reduce oxygenator inlet pressures during ECC. Postoperatively, PC showed to remarkably reduce platelet consumption. Coating showed also to reduce postoperative blood loss, although the difference did not reach statistical significance. No differences between the two groups were found in terms of additional perioperative effects. The use of PC in low-risk elective cardiac surgery patients enhances ECC management, by means of a less restrictive trans-oxygenator blood flow. 009 Published by European Association for Cardio-Thoracic Surgery. All rights reserved. Keywords: Extracorporeal circulation; Artificial surface coating; Platelet consumption; Cardiac surgery; Phosphorylcholine coating 1. Introduction Extracorporeal circulation (ECC) has been demonstrated to induce complex systemic inflammatory response w1x and to affect peculiar aspects of the hematological system, significantly contributing to several adverse postoperative complications wx. Much effort was undertaken in recent years to reduce ECC-related adverse events w3x and to develop more physiological or more biocompatible ECC materials w4 7x. Heparin-coated (HC) and, more recently, phosphorylcholine coated (PC) circuits have been demonstrated to reduce inflammatory response w8x. Nonetheless, the activation of blood components does not exclusively account for postoperative complications. Indeed, the contact of blood elements with artificial surfaces soon after ECC institution (particularly at the level of the oxygenator membranes and heat exchanger) is known, in a few cases, to elicit a sudden thrombotic phenomenon, denominated high pressure-drop (HPD) w9, 10x. This condition, due to exaggerated platelet activation, although not entirely elucidated, is directly linked to Supported by Associazione Cuore e Ricerca. *Corresponding author. Tel.: q ; fax: q address: roberto_lorusso@iol.it (R. Lorusso). 009 Published by European Association for Cardio-Thoracic Surgery reduced oxygenator performance, high resistance to pump flow, increased hemolysis due to red cell trauma, and, ultimately, to ECC failure to efficiently sustain oxygenation and circulation, requiring emergency oxygenator changeover w10x. To our knowledge, however, few studies w11x exist focusing on the impact of such an oxygenator coating in terms of ECC management and course, which play critical roles in terms of eliciting factors for inflammatory response, coagulation impairment, and whole body reaction. Therefore, the aim of this study was to evaluate the effects of phosphorylcholine coating (PC) on intra-operative extracorporeal circulation (ECC) management and perioperative outcome.. Patients and methods.1. Patient population One hundred and twenty consecutive cardiac surgery patients were prospectively enrolled for the study. Inclusion criteria were: elective surgery, absence of hematological or hepatic disorder, absence of chronic obstructive pulmonary disease, no history or recent (-3 weeks) acute pulmonary edema, absence of antiplateletyheparinyother anticoagulation therapy (-7 days). Exclusion criteria were: presence of severe kidney disease, indication for major
2 8 R. Lorusso et al. / Interactive CardioVascular and Thoracic Surgery 8 (009) 7 11 vascular aortic or cardiac surgery and need for combined non-cardiac surgery. Patients were randomly assigned to ECC circuit with PC oxygenator (PC group, 60 patients, of whom 30 subjects with Avant D 903 Physio, Dideco, Sorin group, Mirandola, Italy, and 30 subjects with Monolith Mimesis, Sorin Biomedical, Sorin group, Saluggia, Italy, respectively) or to the corresponding uncoated oxygenator (NPC group, 60 patients, of whom 30 subjects with Avant D903, Dideco, Mirandola, Italy, and 30 subjects with Monolith, Sorin- Biomedical, Sorin group, Saluggia, Italy, respectively). Patient characteristics and surgical details are presented in Table 1. No differences were found between PC and noncoated groups in terms of demographics, operative as well as preoperative hematological profiles. Furthermore, the coagulation status at baseline was comparable between groups (Table 1). No differences were also found comparing the four different subgroups. The majority of patients (45 patients in PC group and 38 in non-coated group, respectively) had an ECC time F70 min (range min). Prolonged ECC (G70 min) was recorded in 15 patients (5%) of PC and (36.6%) of non-coated group (Ps0.)... Ethical issues An informed consent was obtained preoperatively from each patient for the use of their personal data for scientific purposes according to the Helsinki Declaration. The study was approved by the Institutional Ethics Board. The authors had full access to the data and take responsibility for its integrity..3. ECC management Cardiopulmonary bypass (atrio-aorta cannulation) was instituted after systemic heparinization (porcine heparin Table 1 Patient demographics and surgical details PC NPC P-value Age, year 69"10 66"9 0. Gender MyF 47y13 (78.4y1.6) 50y10 (83.3y16.7) 0.08 BSA (m ykg) 1.81" " Coagulation data PT 80"7 86"9 0. INR 1.0"0. 1.1" aptt 8"6 6"8 0.4 FBG 96"57 314" PLT 0"37 35" Surgery CABG 45 (75) 45 (75) Valve 9 (15) 10 (16.6) 0.9 CABGqvalve 6 (10) 5 (9.4) ECC time (min) 70"13 70"14 )0.9 CCL time (min) 53"9 50"1 0.6 Preoperative 36"5 37"5 0.9 hematocrit (%) Continuous variables are presented as mean"s.d.; Discrete variables are presented as percentage (parentheses). PC, phosphorylcholine coating; NPC, non-phosphorylcholine coating; MyF, maleyfemale; BSA, body surface area; PT, prothrombin time (%); INR, international normalized ratio; aptt, activated prothrombin time (s); FBG, fibrinogen (mgydl); PLT, platelets count 9 (n=10 yl). CABG, coronary artery bypass grafting; ECC, extracorporeal circulation; CCL, (aortic) cross-clamp. 300 IUykg; Roche Pharmaceutical, Mannheim, Germany). Activated coagulation time (Kaolin ACT, Medtronic Memo Tech, Inc, Englewood, CO, USA) was maintained above 400 s during ECC. No autologous blood donation was performed preoperatively. Priming (total 1500 cc) was achieved with saline solution (1400 cc), mannitol (50 cc) and NaHCO 3 (50 cc). Additional 50 mg of heparin were constantly added to priming solution. Additional heparin was administered whenever ACT was below 400 s during ECC. Body temperature was kept constant at 3 8C during all the procedures. Cold crystalloid cardioplegia (St. Thomas Hospital) was used in all the procedures (range of cardioplegic solution volume from 700 to 100 cc). Cardiac venting was achieved by aortic root (coronary artery bypass grafting, CABG), or main pulmonary artery venting (valve or combined surgery). Trans-oxygenator pressure drop (pre- and post-oxygenator pressure monitoring) and pump blood flows were recorded every 10 min (Stockert Automatic On-Line Pressure Transducer System, Dideco-Stockert, Munchen, Germany). Inlet and outlet oxygenator pressure recording was calibrated in all patients just after priming maneuver (0 value achieved with no pump flow, before ECC institution). Pressure transducers were allocated exactly at the same levels of inlet or outlet port. Additionally, blood gases and hematological parameters were recorded during surgery before ECC institution and every 10 min thereafter until ECC discontinuation. Optimal blood oxygenation was considered with PaO of mmhg and PaCO of mmhg. PaO and PaCO values were obtained in all patients with 50% of FiO, and gas flowyblood flow ratio of 0.5yl, respectively. The target pump flow was.5 lyminy m BSA..4. Transfusion protocol Blood products were given, when necessary, following an accepted transfusion protocol w1x: Red blood cells (RBCs) to maintain the hemoglobin concentration G7 gydl during ECC and G9 gydl during the postoperative period mlykg of fresh-frozen plasma (FFP) when prothrombin time (PT) )1.5 times the control values. One unit of pooled PLT concentratesy10 kg body weight..5. Data collection Patient variables were recorded at operating room arrival, at Intensive Care Unit arrival, at 4 and 48 h after surgery. Oxygenation inlet pressure (mmhg), oxygenation outlet pressure (mmhg), pump flow (lymin), arterial PCO, mean systemic arterial pressure (mmhg), and hematocrit (%) were collected 10 min after extra-corporeal circulation start (T ), and every 10 min afterwards (T T ). Because 1 6 of the limited number of patients who had undergone prolonged ()60 min) ECC, intra-operative data are presented until T (60 min of ECC) Sample size and randomization The sample size was determined by Graph Pad Stat Mate release.00 (Graph Pad Prism Software, Inc, San Diego,
3 R. Lorusso et al. / Interactive CardioVascular and Thoracic Surgery 8 (009) CA) on the basis of the following assumptions: type I error of 0.05 (two-sided), power of 80%, difference in oxygenator inlet pressure of 14.9 mmhg, standard deviation of 5 mmhg (obtained by 10 patients w5 PC, 5 NPCx not included in the study). The calculated study population was 10. Randomization was carried out by Stats Direct for Windows, release.3.8 (Stats Direct Ltd, Cheshire, UK). The allocation sequence was generated by S.G.; S.R. enrolled participants and S.B. assigned participants to their Group. Surgeons and anesthesiologists were blinded to the type of oxygenator (coated or not coated) used during ECC..7. Statistical analysis Continuous variables are presented as mean and standard deviation (S.D.), categorical variables as percent. Comparisons were carried out using two-sided Student s t-tests for parametric data, Mann Whitney U-test for non-parametric data and x -test or Fisher exact test for categorical variables. Variable changes at T 1 T6 were analyzed by ANOVA with Tukey post-hoc test. SPSS 1.0 (SPSS, Chicago, IL, USA) and Stats Direct.5.7 (Stats Direct, Sale, UK) were used for these calculations. Significance for hypothesis testing was set at the 0.05 twotailed level. 3. Results There were three hospital deaths without any significant difference between groups (one sepsis and two acute respiratory distress syndrome wardsx, two in the non-coated group and one in the PC group, respectively). Phosphorylcholine coating showed to significantly (P-0.01) reduce trans-oxygenator pressure drop during ECC (Fig. 1a). No difference was present cross-matching the two types of PC or the two non-coated oxygenators (Fig. 1b). Arterial PaO reduced significantly during ECC in the NPC group whereas it remained constant in PC group (Fig. 1c). Furthermore, in 1 cases of non-coated circuits and in three cases of PC, increase in FiO (80%) was mandatory because of reduced blood oxygenation at standard O flowypump flows ratio, with subsequent resolution of relative hypoxemia. Hematocrit did not change during ECC and was not different in the two groups (Fig. 1d). Phosphorylcholine-treated oxygenators also showed to generate lower resistance to flow, as documented by lower inlet oxygenator pressures (Fig. a), higher outlet pressure, higher pump flows and higher arterial systemic pressure (Fig. b d) at corresponding pump flows. Notwithstanding, in the non-coated group there were 0 cases of inlet pressure above 350 mmhg and nine cases above 400 mmhg, as compared with two cases and no case with such values, respectively, in PC group. The condition of high inlet pressure resulted in exacerbated pressure drop and to marked hypoxemia with the ultimate need of oxygenator changeover which occurred in one patient (non-coated group). Analysis of dysfunctional ECC circuit was performed and massive thrombosis of heat exchanger and hollow fibers was dramatically evident. In terms of perioperative assessment, PC showed to reduce postoperative platelet consumption after ECC (175"54=10 Uyl vs. 148"49=10 Uyl, Ps0.0) at one (198"7=10 Uyl vs. 160"40=10 Uyl, Ps0.006) and two day (166"51=10 Uyl vs. 153"39=10 Uyl, Ps0.009) without any difference between the two PC subgroups post, or between the two non-coated subgroups. Although apparent better coagulation conditions, patients submitted to PC ECC did not show substantial benefit in terms of postoperative bleeding, even if a trend towards less blood loss was recorded. In contrast, a beneficial effect of PC was documented in terms of reduced incidence of transfused patients as well as reduced amount of blood products used (Table ). 4. Discussion In recent years, different strategies have been proposed aimed at improving the biocompatibility of ECC systems by means of less contact activation of blood elements and thereby less inflammatory response. The application of heparin to ECC surface, either covalently or ionically-bonded, has been tested with initial promising results particularly in high-risk patients w13x, although controversies still persist in terms of actual benefits from the clinical standpoint w14x. Recently, in an attempt to more closely reproduce the natural milieu of the inner vascular layer, and to avoid recognition by the blood as foreign material, phosphorylcholine coating (PC) has been introduced as an innovative approach for extracorporeal surface treatment w7, 8x. Abnormal high preoxygenator pressures, however, may occur w9, 10x and this unfavorable event has been claimed to be generated by platelet deposition upon the oxygenator surface, usually leading to reduced oxygenation efficiency and blood element trauma. In most instances, this phenomenon is usually self-limiting and most of the time also with no detectable phenomena. In a few cases, however, this condition may have remarkable consequences, ultimately leading to unsustainable high pre-oxygenator pressure, arterial hypoxemia, and macroscopic hemolysis, with obvious need of oxygenator change-out. Erica Jansson, a Swedish perfusionist, was the first describing a phenomenon where an increase in oxygenator s inlet pressure occurs despite adequate heparinization w15x. This dangerous condition has been subsequently reported with rising frequency, and many factors have been proposed as predisposing factors w9x. ECC surface coating may, therefore, represent a critical factor not only in the light of high-pressure drop avoidance, but also to enhance pump flow across oxygenator. It must be taken into account that although uneventful ECC management and procedure is the rule, high inlet pressures and high-pressure drops represent well defined traumatic factors to blood cells and, through augmented shear stress, may exacerbate inflammatory pathways and complement activation. In our series, PC showed, at equal pump flows, to significantly (P-0.01) attenuate pressure drop across oxygenators and to reduce oxygenator inlet pressures during ECC irrespective of the type of oxygenator. Furthermore, PC showed to remarkably reduce platelet consumption, and a lower incidence of blood transfusions as well was also documented in PC group. Coating showed also to reduce
4 10 R. Lorusso et al. / Interactive CardioVascular and Thoracic Surgery 8 (009) 7 11 Fig. 1. (a) Comparison between trans-oxygenator pressure drop obtained with coated and conventional circuit. Pressure assessments are presented for the first ECC hour (T 1 T 6, monitoring every 10 min). Bars: standard deviation. *P-0.05, **P (b) Circuit type-adjusted pressure-drop across the oxygenators. No difference was found between PCO oxygenators or between non-coated oxygenators. ns: not significant. (c) Arterial PaO (a) and (b) Hematocrit (HT) in the two groups. See text. *P-0.05 vs. PC group. Bars: standard deviation. Fig.. (a d) Comparison between group about extracorporeal circulation (ECC) parameters. See text. *P-0.05 vs. PC group. postoperative blood loss, although the difference did not reach statistical significance Limitations of the study Our study should be viewed in light of some inherent limitations. The study was performed in a limited number of patients. ECC circuits were not entirely (tip-to-tip) coated with phosphorylcholine (only the oxygenator was coated) and were open. Despite an evident limitation in terms of actual biocompatible ECC, the absence of a global coating may have blunted the effects of PCO and, therefore, underestimated its actual benefits. The aspirated blood was not discarded and it has been reported to be a major determinant of the pro-inflammatory response following ECC. However, likely due to the smaller number of such patients, also the procedure-adjusted analysis did not modify final results, suggesting that the influence of sucked field blood acts predominantly on complement activation because of tissue factor action, and hence on the inflammatory reaction rather than on surface-related pathways. The arterial pressure was not manipulated pharmacologically, but individual adrenergic hormonal response
5 R. Lorusso et al. / Interactive CardioVascular and Thoracic Surgery 8 (009) Table Postoperative outcome PC NPC P-value Bleeding 537"84 661" Plasma creatinine Preoperative 1.03"0. 0.9" Post ECC 0.9"0 0.9" st postoperative day 1.1" " nd postoperative day 1." " Atrial fibrillation, n 7 (11.6) 13 (1.6) 0.06 Transfusion, n 6 (10) 1 (35) Transfusion, Uypt 0.4" " Continuous variables are presented as mean"s.d. (parentheses); Discrete variables are presented as percentage (parentheses). PC, phosphorylcholine coating; NPC, non-phosphorylcholine coating; Uypt, units per patient. might have played a role in the determination of mean arterial pressure therefore not actually representing the effect of a more or less efficient oxygenator performance at equal pump flows. No analysis of the inflammation reaction was performed; this will be the object of ongoing research. 5. Conclusions In conclusion, PC oxygenator seems to enhance a more efficient ECC management by means of a less restrictive trans-oxygenator blood flow. However, whether the coating of the oxygenator really changes anything in the management and the postoperative outcome of patients is still an open issue. Further studies are required to confirm our findings. Acknowledgments We gratefully thank Dr Orlando Parise for statistical analysis and Dr Judith Wilson for the English revision of the paper. References w1x Laffey JG, Boylan JF, Cheng DC. The systemic inflammatory response to cardiac surgery: implications for the anesthesiologist. Anesthesiology 00;97:15 5. wx De Somer F, Van Belleghem Y, Caes F, Francois K, Van Overbeke H, Arnout J, Taeymans Y, Van Nooten G. Tissue factor as the main activator of the coagulation system during cardiopulmonary bypass. J Thorac Cardiovasc Surg 00;13: w3x Weiland AP, Walker WE. Physiologic principles and clinical sequelae of cardiopulmonary bypass. Heart Lung 1986;15: Erratum in: Heart Lung 1986;15:465. w4x von Segesser LK. Surface coating of cardiopulmonary bypass circuits. Perfusion 1996;11: w5x von Segesser LK. Safety and efficacy of heparin-bonded surfaces in cardiopulmonary bypass. J Thorac Cardiovasc Surg 001;11: w6x von Segesser LK. Heparin-bonded surfaces in extracorporeal membrane oxygenation for cardiac support. Ann Thorac Surg 1996;61: w7x von Segesser LK, Tönz M, Leskosek B, Turina M. Evaluation of phospholipidic surface coatings ex-vivo. Int J Artif Organs 1994;17: w8x De Somer F, Francois K, van Oeveren W, Poelaert J, De Wolf D, Ebels T, Van Nooten G. Phosphorylcholine coating of extracorporeal circuits provide natural protection against blood activation by the material surface. Eur J Cardio-Thorac Surg 000;18: w9x Blombäck M, Kronlund P, Aberg B, Fatah K, Hansson LO, Egberg N, Moor E, Carlsson K. Pathologic fibrin formation and cold-induced clotting of membrane oxygenators during cardiopulmonary bypass. J Cardiothorac Vasc Anesth 1995;9: w10x Wahba A, Philipp A, Behr R, Birnbaum DE. Heparin-coated equipment reduces the risk of oxygenator failure. Ann Thorac Surg 1998;65: w11x Mueller XM, Tevaearai HT, Augstburger M, Horisberger J, von Segesser LK. Experimental evaluation of the Dideco D903 Avant 1.7 hollow-fibre membrane oxygenator. Perfusion 1998;13: w1x Nuttall GA, Stehling LC, Beighley CM, Faust RJ. American Society of Anesthesiologists Committee on Transfusion Medicine. Current transfusion practices of members of the American Society of Anesthesiologists: a survey. Anesthesiology 003;99: w13x Weiss BM, von Segesser LK. Pro and con of heparin-bonded circuits for cardiopulmonary bypass. J Cardiothorac Vasc Anesth 1999;13: w14x Horton SB, Butt WW, Mullaly RJ, Thuys CA, O Connor EB, Byron K, Cochrane AD, Brizard CP, Karl TR. IL-6 and IL-8 levels after cardiopulmonary bypass are not affected by surface coating. Ann Thorac Surg 1999;68: w15x Jansson E. Casualty due to fibrin discharge in oxygenators. Scanmag 1990;3:13 14.
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