TY - JOUR
AU - Mankad,, P.S.
AB - Abstract Objective: The merits of centrifugal pump in adult cardiopulmonary bypass are well established. This study compares the effects of the Medtronic Biomedicus centrifugal pump with conventionally used roller pump in routine cardiopulmonary bypass in infants and children. Methods: Between June 1996 and March 1997, 42 children (aged 2 days–13 years) undergoing elective cardiac surgery were assigned to either centrifugal or roller pump bypass. The following variables were studied: haemolysis (haematocrit, free plasma haemoglobin, haptoglobins), platelet activity (platelet counts, Beta-thromboglobulin), leukocyte count, cytokine release (IL-2, IL-6, IL-8), complement activation (C3a and C5a), blood and blood product requirements, urine output on bypass, post-operative blood urea, duration of ventilation, intensive care and hospital stay. Results: Age, weight, disease complexity, duration of bypass, and a number of other variables were comparable in the two groups. The centrifugal pump resulted in lower plasma free haemoglobin (mean±SD, 50±23 vs. 72±35 mg/dl, P<0.01), higher platelet count (133.1±34.8 vs. 63.5±29.6×109/l, P<0.01), less platelet activation (β-TG 1253±633 vs. 1657±677 ng/ml; P<0.05), less cytokine release (IL-6 329±57 vs. 392±59 pg/ml; P<0.05), and reduced levels of C3a (4822±274 vs. 5933±393 ng/ml, P<0.01). Differences were detected in favour of the centrifugal pump in urine output on bypass (4.1±0.5 vs. 2.3±1.9 ml/kg per h, P<0.01), post-operative maximal urea (6.5±3.1 vs. 10.2±6.7 mmol/l, P<0.02), ventilation time (18.9+6.5 vs. 56.5+51.7 h, P<0.01), duration of intensive care (1.4±0.79 vs. 3.33±2.8 days, P<0.05) and hospital stay (5.7±1.4 vs. 15.75±23.9 days, P<0.01), but not in blood and blood product requirements (RCC: 11.26±4.6 vs. 10.77±4.2 ml/kg per 24 h, P>0.05). Conclusion: The centrifugal pump as compared to roller pump results in less blood trauma, reduced platelet activation and less pronounced inflammatory response. There is also an improved renal response during and after bypass. This is translated clinically into reduced requirement for ventilation, shorter intensive care and hospital stays. These results strongly favour the use of centrifugal pump in routine paediatric cardiac surgery. Centrifugal, Roller, Cardiopulmonary bypass, Haemolysis, Cytokine, Platelets, Complement, Interleukin Introduction The aetiology of cardiopulmonary bypass (CPB) induced damage to blood components, coagulopathy and inflammatory response is multifactorial [1],[2],[3],[4]. A roller pump, used conventionally in CPB, is one of the important factors contributing to these adverse effects. In an attempt to limit the damaging effects from bypass, various investigators have studied less traumatic blood pumps, i.e. centrifugal pumps, in adult patients [5],[6],[7],[8],[9]. However, the findings from adult studies cannot be directly extrapolated to children as centrifugal pumps have been shown to behave differently under varying pressure and flow situations [10],[11]. This is shown in a recent study comparing roller with centrifugal pumps in in-vitro circuits designed to simulate the neonatal circulation which concluded that there was no difference in the rate of haemolysis [12]. Furthermore, despite the fact that neonates and children are even more susceptible to this ‘postperfusion syndrome' the role of a centrifugal pump has not been adequately addressed in this group of patients The objective of this study was to investigate the haemolysis, platelet damage, and immunological activation in a randomised prospective trial comparing centrifugal with roller pump. The correlation between these haematological and biochemical parameters to the early clinical outcome was also evaluated. Materials and methods Patients Forty-two children attending for elective open-heart surgery at a single institution were enrolled in this prospective randomised study. Patients were randomly allocated to receive cardiopulmonary bypass using either the Stockert roller pump or Medtronic Biomedicus centrifugal pump. Randomisation was achieved by opening a sealed envelope after obtaining informed consent for the study. Patients were excluded from participation in the trial in the presence of any of the following: known pre-operative haematological disorder, suspected preoperative infection, or emergency surgery. However, during the course of the study, we did not encounter any patients who would have been excluded on the basis of these criteria. Informed consent was obtained by an investigator not directly involved in the surgery, from one or both parents/guardians of the child. The local and hospital ethics committees granted permission for this work. Standardised anaesthetic technique was employed throughout. Phenoxybenzamine was administered prior to bypass (1 mg/kg) in patients with raised pulmonary arterial pressures pre-operatively. Cardiopulmonary bypass circuit components were: flexible venous reservoir, cardiotomy reservoir (Avecor Cardiovascular Ltd., Bellshill, UK), membrane oxygenator (Solid silicone membrane type: 0400, 0800, 1500–2A), roller pump (Stockert Instruments, Munich, Germany) or Biomedicus centrifugal pump (BP50 or BP80; Medtronic, Minneapolis, MN, USA). A blood-based pump prime was utilised. Surgery was performed on all patients by the same surgeon using, as far as was feasible standardised techniques. Moderate hypothermia of 25–28°C was usual. Cardiotomy/vent suction was minimised, although in a few cases this was close to 2% of calculated flow rates. Aortic cross-clamping was utilised with antegrade crystalloid cardioplegia (St. Thomas' Hospital solution) cooled to 4°C. Bypass was weaned in the usual fashion after which heparin was reversed with protamine 3 mg/kg as a slow IV infusion. Patients received blood in the pump prime, on bypass and off bypass strictly to maintain a haematocrit between 35 and 40% in the post-operative period. This was uniform for both groups. Modified ultrafiltration was performed after bypass with a haemofilter (Cobe Cardiovascular) to achieve a haematocrit of greater than 35%. All children received 10 ml/kg of platelet concentrate and 10 ml/kg fresh frozen plasma (FFP) as routine, following protamine administration but prior to chest closure. Additional doses of blood products including cryoprecipitates were transfused in the ITU depending upon the clinical indication and results of coagulation screen. Postoperative haematocrit values were maintained between 35 and 40% by red cell concentrate (RCC) transfusion. Blood sampling Blood samples were withdrawn at induction of anaesthesia, at the end of bypass, and after 1, 2 and 20 h following cessation of the bypass. Blood was collected in tubes appropriate to the analyses being performed. Haematology samples were transported to the laboratory for centrifugation and freezing to −70°C for later batch analysis. Immunology samples were centrifuged immediately after collection, and the supernatant divided and frozen at −70°C. Laboratory analysis Free plasma haemoglobin was measured by spectrophotometric analysis (Sigma, St. Louis, MO, USA) [13]. Plasma haptoglobin levels were determined by radial immunodiffusion (Kent, Richmond, WA, USA). Full blood count analysis (WBC, RBC, Hb, Hct, MCV, Plt) was by automated Coulter counter. Beta-thromboglobulin (β-TG) was measured by a competitive radioimmunoassay technique (Amersham, UK) [14]. Complement factors C3a and C5a were measured using competitive two-step 125I-labelled radioimmunoassay (Amersham, Buckinghamshire, UK) [15]. Interleukins IL-2, IL-6, IL-8 were analysed using a solid phase sandwich enzyme immunoassay technique (ELISA; R and D Systems Europe, Abingdon, UK) [16],[17]. Evaluation quality criteria. These tests are well standardised in our laboratories and are used extensively in neonatal and paediatric research of the departments of Child Life and Health, and Clinical Haematology. Both laboratories involved in processing samples from this study performed rigorous quality control analyses. The results of these tests were entirely satisfactory. Statistical analysis After tabulating the data, statistical analysis was performed using Microsoft Excel 97 SR-1. Transformation of the raw data was performed by expressing each study value as a percentage of baseline (pre-operative) levels. Single factor analysis of variation was then used to compare centrifugal pump group against roller pump group, using baseline levels as a control. Non-parametric data were analysed using the Wilcoxon Rank Sum test. Data are the mean±SE. A P-value of less than 0.05 was considered significant. Results Of the 42 children initially enrolled in the study, three were subsequently excluded due to one death within the first 24 h, and two children were unable to complete the study on account of their procedures extending beyond laboratory sampling hours. The two groups were comparable in terms of, age, sex weight and cardiopulmonary bypass time as there was no statistically significant difference in the composition of the groups in relation to these parameters (Table 1 ). The types of operations in each group were naturally quite varied. Simple cases such as ASD repairs were excluded. The distribution of intermediate and complex cases was similar between the groups. Table 1 Open in new tabDownload slide Patient characteristics Table 1 Open in new tabDownload slide Patient characteristics Haematology Free plasma haemoglobin Maximal plasma free haemoglobin levels occurred at the end of bypass and fell slowly thereafter, almost reaching baseline after 24 h. This elevation was most pronounced in the roller pump group with significantly elevated levels also at 1 h (66±10.9 vs. 19±14.4 mg/dl, P<0.01; Fig. 1 ). Banked blood prime could be a potential source of experimental error, should there be any haemolysis in the stored blood. Free haemoglobin was measured in pump prime by obtaining a single sample prior to bypass. The mean free Hb concentration for roller pump was 13.7 mg/dl (range 3.5–29.2, ±2.1 mg/dl) and for centrifugal pump, 14.5 mg/dl (range 4.9–24.9, ±1.9 mg/dl). There was no significant difference between the groups. Fig. 1 Open in new tabDownload slide Plasma free haemoglobin levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at end of bypass and bypass+1 h (P<0.01). Fig. 1 Open in new tabDownload slide Plasma free haemoglobin levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at end of bypass and bypass+1 h (P<0.01). Haptoglobins The plasma haptoglobin level is a sensitive indicator of haemolytic activity within blood, scavenging free haemoglobin molecules. In virtually all samples after the commencement of bypass, plasma haptoglobin levels fell to levels below the limits of detection of the test (<0.1 g/l). This suggests that the amount of free haemoglobin overwhelmed the ability of haptoglobin to deal with this degree of haemolysis in both groups. Haematocrit Haematocrit decreased significantly at the end of bypass in both groups (roller: 0.32±0.06 vs. centrifugal: 0.31±0.05%) from baseline levels (0.39±0.09 vs. 0.40±0.08%) but there was no significant difference between the groups. This reflects haemodilution, which is normally present at the end of bypass, and was corrected by ultrafiltration and red cell concentrate transfusion as required. Red cell haemoglobin concentration and total haemoglobin exhibited a similar decrease at the end of bypass, thereafter returning to baseline values by 20 h post-CPB. There was no significant statistical difference between the groups. Platelets Platelet counts fell substantially after bypass in both groups. This reached a nadir at 1 h then increased towards, but remaining 50% below, baseline values. This drop in platelet count was less pronounced in the centrifugal pump (32.5±8.7 vs. 67±7.2×109/l), reaching statistical significance at end of bypass (P<0.01) and CPB±1 h (P<0.05; Fig. 2 ). Fig. 2 Open in new tabDownload slide Platelet counts for roller pump (—) and centrifugal pump(…) groups. Statistically significant at end of bypass (P<0.01) and bypass+1 h (P<0.05). Fig. 2 Open in new tabDownload slide Platelet counts for roller pump (—) and centrifugal pump(…) groups. Statistically significant at end of bypass (P<0.01) and bypass+1 h (P<0.05). Beta thromboglobulin Grossly elevated β-TG levels were seen in both groups, remaining elevated post-operatively and falling slowly towards baseline values. At 20 h the levels were still over 50% peak values. There was a small statistically non-significant difference between the groups at the end of bypass (2021±233 vs. 1871±213 ng/ml, 0.1>P>0.05), but becoming significant at 1 and 20 h (P<0.05; Fig. 3 ). Fig. 3 Open in new tabDownload slide Beta thromboglobulin levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at end of bypass (P<0.05) and bypass+1 and 2 h (P<0.05). Fig. 3 Open in new tabDownload slide Beta thromboglobulin levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at end of bypass (P<0.05) and bypass+1 and 2 h (P<0.05). WCC In the roller pump group white cell count initially fell to below baseline level by the end of bypass but subsequently continued to rise then plateau after 24 h. This initial fall was not observed in the centrifugal group, who exhibited a steady rise from baseline level (8.46±0.79×109/l) for 2 h (12.3±1.1×109/l) then plateaued. Comparison between groups reached statistical significance at the end of the bypass and after 1 and 2 h post-CPB (P<0.01; Fig. 4 ). Fig. 4 Open in new tabDownload slide White cell counts for roller pump (—) and centrifugal pump groups (…). Statistically significant at end of bypass and bypass+1 h (P<0.01) and bypass+2 h (P<0.05) Fig. 4 Open in new tabDownload slide White cell counts for roller pump (—) and centrifugal pump groups (…). Statistically significant at end of bypass and bypass+1 h (P<0.01) and bypass+2 h (P<0.05) Complement factors C3a Levels of C3a were elevated at the end of bypass but continued to rise peaking after 1 h, plateauing between 1 and 2 h, then with partial return to baseline values at 20 h. Statistically significant differences were detected between groups at CPB±1 h (roller: 5886±260 vs. centrifugal: 4699±173 ng/ml, P<0.01) and 2 h (5933±393 vs. 4822±274 ng/ml, P<0.01). (Fig. 5 ). Fig. 5 Open in new tabDownload slide (a) C3a levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at bypass+1 and 2 h (P<0.01). (b) IL-6 levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at bypass+2 h (P<0.05). Fig. 5 Open in new tabDownload slide (a) C3a levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at bypass+1 and 2 h (P<0.01). (b) IL-6 levels for roller pump (—) and centrifugal pump groups (…). Statistically significant at bypass+2 h (P<0.05). C5a In many of the patients C5a was not detected at the lowest limits of the test. In those in whom levels were detected, low level elevation was observed which mirrored the C3a profiles. No significant differences were detected between roller and centrifugal groups. Cytokines IL-6 and IL-8 Both these active cytokines were elevated following bypass and continued to rise after 2 h, falling to near baseline levels by 20 h. Significant differences were observed between groups for only IL-6 at CPB±2 h (roller: 392±59 vs. centrifugal: 329±57 pg/ml, P<0.05; Fig. 5). IL-2 In a similar fashion to C5a, many patients showed no rise in IL-2 levels either at the end of bypass or subsequently. Sporadic elevations were detected in some patients but without any recognisable pattern. No further analysis was performed on this data. Clinical outcome (Table 2) Table 2 Open in new tabDownload slide Transfusion data and clinical outcomes for roller and centrifugal pump groups Table 2 Open in new tabDownload slide Transfusion data and clinical outcomes for roller and centrifugal pump groups Blood and blood product transfusion The total transfusion requirements of red cell concentrate, platelet concentrate, fresh frozen plasma and cryoprecipitates were measured over the first 24 h. We analysed the total transfusion requirement in the two groups, which included pump prime, on bypass and post-bypass. Both groups were managed in a similar fashion on bypass, therefore, there was no significant difference in their transfusion requirements, in pump prime and in blood added to the pump during bypass. Small differences were observed between groups with respect to administration of blood products, with FFP reaching statistical significance (centrifugal: 13.0±2.7 vs. roller: 30.4±9.3 ml/kg per 24 h, P<0.05). Urine output on bypass and post-operative blood urea The urine output was standardised for body weight and time on bypass, and expressed in ml/kg per h. A significantly greater urine output was observed in the centrifugal group (4.1±1.4 vs. 2.3±0.5 ml/kg per h, P<0.01). Post-operatively, in the majority of cases there was an elevation in the plasma urea concentration, however, this was less pronounced in the centrifugal pump group (6.5±3.1 vs. 10.2±6.7 mmol/l, P<0.02). Pre and post-operative creatinine levels correlated with the urea (roller r=0.85, centrifugal r=0.84). This elevation was more pronounced in the roller group (pre-operative 53.7±2.1 vs. post-operative 63.1±5.5 μmol/l) compared with the centrifugal group (pre-operative 56.7±1.8 vs. post-operative 62.1±4.3 μmol/l). Hospitalisation This data was skewed because three children in the roller pump group had markedly increased ventilation time and ITU stay. Overall, ventilation time (18.9±6.5 vs. 56.5±51.7 h, P<0.01), and intensive care stay (1.4±0.8 vs. 3.3±2.8 days, P<0.05) were shorter in the centrifugal group, with shorter hospital stay (5.7±1.4 vs. 15.8±23.9 days, P<0.01). There was no correlation between ventilation time and B-TG (roller: r=0.07; centrifugal: r=0.67), C3a (roller: r=0.52; centrifugal: r=0.75), or IL-6 (roller: r=0.43; centrifugal: r=0.13). However, of those patients ventilated for 5 days or longer, there were correspondingly greater elevations in B-TG (2213±615 vs. 1253±633 ng/ml; P<0.05), C3a (9070±2369 vs. 4822±274 ng/ml; P<0.05) and IL-6 (393±163 vs. 329±57 pg/ml; NS) when compared with the centrifugal group. Discussion This study demonstrates that the centrifugal pump is superior to the roller pump for routine cardiopulmonary bypass in children. There was less cellular damage reflected by lower red cell haemolysis and maintenance of platelet and leukocyte counts. Platelet activation was significantly lower resulting in lower levels of β-TG. Complement and cytokine levels were lower resulting in less activation of the immune system. A number of in-vitro and clinical studies in adults have shown the superiority of a centrifugal pump over a roller pump in terms of haemolysis, complement activation and platelet activation [8],[18],[19],[20],[21]. As a result the use of centrifugal pump for CPB is increasing in adult patients, being currently over 50% in the USA and 15% in Europe [22]. However, there are controversial data regarding the use of centrifugal pump in paediatric CPB. Wheeldon et al. have shown increased haemolysis and fluctuating flow rates with CP in paediatric perfusion [11]. In contrast, Koja et al. have shown significant benefits with the use of centrifugal pump as compared to roller pumps on blood components [9]. This controversy is also echoed in in-vitro studies [10],[12]. Using porcine blood at 21°C, Tamari et al. evaluated the effects of the Bio-Medicus centrifugal pump and roller pumps under different flow and pressure conditions [10]. They concluded that the Bio-Medicus centrifugal pump was most haemolytic in low flow-high pressure applications such as in paediatric CPB, and the roller pump was most haemolytic in high flow-low pressure applications as in adult CPB. Whilst Moon et al. compared in-vitro haemolysis with centrifugal pump and a roller pump at low flow rates, they did not find any significant difference in haemolysis rate between centrifugal pump and roller pump nor between high and low flow applications [12]. None of these in-vivo or in-vitro studies has critically addressed these issues in terms of biochemical markers or clinical outcomes. We observed large elevations in free plasma haemoglobin in both groups suggesting mechanisms for haemolysis other than the pump. However, the centrifugal pump demonstrated significantly lower levels of haemolysis, in contrast to the roller pump where the elevation was sustained after bypass. This suggests lower sublethal red cell damage (i.e. damaged red cells which later lyse, thus contributing to the observed rise in plasma haemoglobin) from the centrifugal pump. Measurement of haptoglobins proved not to be a useful indicator of haemolysis, with the levels becoming undetectable as the haemoglobin-haptoglobin complexes are removed from the circulation by reticulo-endothelial cells. The difference in WCC with the two pumps could be due to increased damage to WCC by roller pump or increased utilisation by cytokine mediated neutrophil–endothelial interaction WBC has been shown to be more vulnerable to mechanical damage by a blood pump than a RBC [23]. The complement activation has been forwarded as a major determinant of the systemic detrimental effects of bypass [24]. In particular C3a, which our study demonstrated in very high quantities especially in the roller pump group, continued to rise after the completion of bypass and is believed to trigger further potentially damaging inflammatory responses. The related species C5a was found in extremely low amounts in the majority of the cases. In part this is due to its short half-life within the circulation, but previous studies have demonstrated binding by lymphocytes [25] and pulmonary sequestration [26]. The unpredictable nature of the IL-6 and IL-8 response is not so easily explained, although both are labile species which may be binding to activated lymphocytes. The modified ultrafiltration performed at the end of bypass may be responsible for removing IL-6 and IL-8 from the circulation, although others have reported elevated levels in patients receiving haemodialysis [27]. The observed haematological and biochemical benefits of CP were equally translated into better clinical outcomes in this group of patients. We observed a difference in urine output on bypass when the centrifugal pump was first used during a pilot study on children in our institution. This study clearly demonstrates better preservation of renal function, as reflected in higher urine output on CPB and lower early post-operative blood urea and creatinine concentrations, despite variations in flow and temperature. Further study into this phenomenon is recommended. Following cardiopulmonary bypass, there occurs a generalised systemic inflammatory response, which has been well described, and termed ‘postperfusion syndrome' [28]. Although this manifests clinically as impairment to a number of organ systems, of particular importance in this context, are the effects on the lungs. Neutrophil activation is believed to be central to this process, resulting in release of further inflammatory mediators such as cytokines, which then amplify the reaction through other mediators such as complement, platelets, kinin and coagulation cascades and endothelium [29]. A central hypothesis of our study is the modulation of this inflammatory response by the type of blood pump used during bypass. The observed reduction in time spent on the ventilator and consequently in intensive care, may be a reflection of less activation of the immune system by the less traumatic centrifugal pump. One of the limitations of our study was the relatively small number of neonates (three in each group) in the two groups. Therefore, we feel that routine use of centrifugal pump in neonatal bypass may need further investigation with larger numbers of patients. However, the data strongly supports the routine use of CP in infants and children over 4 weeks of age. It should also be stressed that the findings of this study may only be applicable to the use of a specific centrifugal pump (Bio-Medicus) evaluated in the trial, as it has been shown that different types of centrifugal pump can cause different amounts of haemolysis based on shear stress, the amount of blood exposure time, and heat generation by mechanical friction [30],[31],[32]. Detailed health economics studies are warranted to analyse the benefits in terms of cost-effectiveness clinically, since the centrifugal pump in our study showed a significant reduction in ITU and hospital stay. In summary, these results strongly support the use of a centrifugal pump in routine paediatric cardiopulmonary bypass procedures. A multi-centre trial enrolling large numbers of newborns is justified to critically address its role in neonatal bypass. Conflict of interest: The Biomedicus centrifugal pump heads were supplied by Medtronic, Minneapolis, MN, USA. None of the investigators, or the institution involved have any financial interest in the manufacturer of this device. 1 Presented at the 11th Annual Meeting of the European Association for Cardio-thoracic Surgery, Copenhagen, Denmark, September 28 – October 1, 1997. Association for Children with Heart Disorders (ACHD); Medtronic; Mrs. Jean Wade, technical officer, Kofi Sedowofia; Professor Neil McIntosh, Department of Child Life and Health, University of Edinburgh; Pam Dawson, Mike Bisland, Chris Ludlam, Haematology Laboratory, Royal Infirmary Edinburgh; the perfusionists: Mrs. Z. Herdis, Mr. C. Robertson, Mrs. D. Aindow; the anaesthetists: Dr. D. Simpson, Dr. I. Hudson, Dr. C. Young, Dr. L. Aldridge; theatre staff and Intensive Care Unit staff of Sick Childrens' Hospital, Edinburgh. Appendix A. Conference discussion Dr D. Vondrys (Prague, Czech Republic): Did you compare the levels of troponin-T in order to gain information about myocardial ischemia? 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TI - Superiority of centrifugal pump over roller pump in paediatric cardiac surgery: prospective randomised trial
JF - European Journal of Cardio-Thoracic Surgery
DO - 10.1016/S1010-7940(98)00067-0
DA - 1998-05-01
UR - https://www.deepdyve.com/lp/oxford-university-press/superiority-of-centrifugal-pump-over-roller-pump-in-paediatric-cardiac-ujYoNsO4zk
SP - 526
EP - 532
VL - 13
IS - 5
DP - DeepDyve
ER -