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Ann Thorac Surg 1996;62:1134-1140
© 1996 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Centrifugal Pump and Heparin Coating Improves Cardiopulmonary Bypass Biocompatibility

Departments of Cardiothoracic Surgery, Anesthesiology, and Clinical Chemistry, Ullevål University Hospital, Oslo, Norway

Accepted for publication May 14, 1996.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. Centrifugal pumps are being used increasingly for short-term extracorporeal circulation purposes such as during heart operations. Whether the centrifugal pump improves the cardiopulmonary bypass biocompatibility has not been fully documented.

Methods. A roller pump (n = 20) was compared in vivo with a centrifugal pump (n = 20) in groups of patients in which cardiopulmonary bypass circuits that were either totally heparin coated (Carmeda BioActive Surface; n = 20) or uncoated (n = 20) were used. We expected the heparin coating to attenuate blood activation, thus possibly making the comparison of the two pumps easier with respect to their different blood activation potentials. Samples of blood plasma, obtained during cardiopulmonary bypass from low-risk coronary artery bypass grafting patients, were analyzed for hemolysis (plasma hemoglobin), complement activation (C3bc and the terminal complement complex), a complement lytic inhibitor (vitronectin), coagulation activation (fibrinopeptide A), granulocyte activation (lactoferrin), and platelet activation (ß-thromboglobulin).

Results. The concentrations of terminal complement complex, lactoferrin, and ß-thromboglobulin were significantly lower in association with heparin-coated surfaces. The concentration of plasma hemoglobin was significantly lower in association with the centrifugal pump. In uncoated circuits, the ß-thromboglobulin level was significantly higher in association with the roller pump than with the centrifugal pump, but this significant reduction in the ß-thromboglobulin level did not hold true for the heparin-coated circuit group.

Conclusions. A heparin-coated cardiopulmonary bypass surface reduces the blood activation potential during cardiopulmonary bypass, and the centrifugal pump causes less hemolysis than the roller pump.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The nonocclusive centrifugal pump was originally constructed for long-term extracorporeal circulation, but has increasingly been used during heart operations. This is probably the result of safety considerations [1] and also its improved blood handling ability [2]. Results from several cardiopulmonary bypass (CPB) model studies have indicated blood activation was reduced in association with the use of systems with a centrifugal rather than a roller pump, and hemolysis was especially reduced in some studies [2, 3]. Reduced complement and platelet activation has also been observed during open heart operations in which centrifugal rather than roller pumps were used [4, 5]. A problem experienced with the centrifugal pump during sustained extracorporeal membrane oxygenation is hemolysis, which has been attributed to the negative pressure on the inlet side [6]. This problem is avoided when a filled venous reservoir is used.

The advent of heparin-coated CPB surfaces has been regarded as an improvement in CPB biocompatibility [7]. Thus, a significant reduction in complement and granulocyte activation has been demonstrated for the Carmeda BioActive Surface heparin-coated CPB [8].

The primary goal of the present study was to compare the effect of the use of a roller or a centrifugal pump on blood activation markers. We expected that the heparin-coated CPB surface would cause blood activation to be attenuated and that lower "background" blood activation would clearly point up differences between the pumps. To study such blood activation, particularly that caused by the pumps, we have assessed heparin-coated and uncoated systems using the following plasma variables: plasma free hemoglobin, reflecting hemolysis; complement activation (C3b, iC3b, and C3c collectively called C3bc, and the terminal complement SC5b-9 complex [TCC]); levels of the complement lytic inhibitor vitronectin; coagulation activation (fibrinopeptide A [FPA]); granulocyte activation (lactoferrin); and platelet activation (ß-thromboglobulin [ß-TG]).

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Forty consecutive patients accepted for elective coronary artery bypass grafting were included in the study after giving informed consent. The exclusion criteria were (1) left ventricular ejection fraction of less than 0.40, (2) any concomitant surgical procedure, (3) chronic obstructive pulmonary disease, renal insufficiency, liver disease, or insulin-dependent diabetes mellitus, (4) a known coagulopathy or ongoing anticoagulation therapy, (5) active inflammatory disease or infection, and (6) use of steroids, nonsteroidal antiinflammatory drugs, or acetylsalicylic acid within 8 days of operation. The patients were placed randomly into one of four groups, with 10 patients in each group:

• Group I: The extracorporeal circuit comprised a roller pump (Gambro, Horten, Norway) and an uncoated oxygenator (Maxima; Medtronic Cardiopulmonary, Anaheim, CA).
  
• Group II: The extracorporeal circuit comprised a Gambro roller pump and a heparin-coated oxygenator (Carmeda BioActive Surface heparin-coated Maxima; Medtronic), with heparin coating of the entire blood-contact surface.
  
• Group III: The extracorporeal circuit comprised a centrifugal pump (Biomedicus; Medtronic) and an uncoated Maxima oxygenator.
  
• Group IV: The extracorporeal circuit comprised a Biomedicus centrifugal pump and Carmeda BioActive Surface heparin-coated Maxima oxygenator, with heparin coating of the entire blood-contact surface.
  

An arterial line filter and a cardiotomy reservoir were used in all patients. We applied the Maxima hollow-fiber membrane oxygenator (model 1380; Medtronic). The cardiotomy reservoirs were a Medtronic Intersept SK 1351, and the venous reservoir, a Medtronic MVR 1600. The arterial filters used were the 20-µm Medtronic Intersept and the prebypass filter, a Medtronic Intersept PBP. In all patients, Medtronic Intersept PVC Class IV tubings were used; the aortic cannula was an AA 024-C and the venous cannula, a TR 3651-0 (Research Medical, Salt Lake City, UT), with either a BioMedicus centrifugal pump (model 540) with an external drive unit (model 540 T) and the Bio-Pump Head (BP 80; Medtronic) or the nonpulsatile Gambro roller pump. The roller pump was adjusted to low occlusion (pressure reduction from 300 to 200 mm Hg in 10 seconds). The temperature control unit was a Gambro Hyper-hypothermia unit (Hyp 10-200; Gambro). Heparin was administered intravenously before the onset of CPB at a rate of 400 IU/kg of body weight (heparin 5,000 IU/mL; Leo, Ballerup, Denmark). Additional heparin was given to achieve a minimum activated coagulation time (ACT) of 480 seconds (reference range, 70–120 seconds). The ACT was measured with a Hemochrome 400 (International Technidyne, Edison, NJ). The operations were performed under moderate general hypothermia (28°–32°C) with topical cooling accomplished by ice slush in addition to cold St. Thomas' cardioplegic solution. After CPB was ended protamine sulfate (10 mg/mL; Leo) was administered to reestablish the preoperative ACT level. Mediastinal shed blood was retransfused. The amount of heparin and protamine administered, the ACT values, the mediastinal blood loss, and the retransfused blood volumes during the first 12 postoperative hours were recorded in all patients.

A baseline sample of blood was obtained from the arterial line at the start of extracorporeal circulation. The test samples were drawn 30 minutes after the start of bypass, 10 minutes after release of the aortic cross-clamp, 10 minutes after the administration of protamine, at skin closure, and 6 hours postoperatively. The blood was sampled in an ethylene-diamine tetraacetic acid vacutainer for routine hematologic analysis, including measurement of the levels of plasma hemoglobin, complement activation products, vitronectin, and lactoferrin. The plasma samples were stored at -70°C before analysis in batches. Samples for analysis of FPA were collected in special vacutainers with a 1/10 volume (0.2 mL) strong inhibitor: 0.15 mol/L of NaCl, 1,000 IU/mL of heparin, and 1,000 IU/mL of aprotinin (Trasylol; Bayer AG, Leverkusen, Germany), centrifuged at 4°C (1,900 x g for 30 minutes), and the plasma was stored at -70°C before analysis in batches. Samples for ß-TG analysis were drawn in special vacutainers, which were ice cooled before sampling and contained 0.2 mL of anticoagulant from Diatube H (Stago; Boehringer Mannheim, Mannheim, Germany). Plasma for ß-TG analysis was obtained from the midlayer to avoid collecting light platelets, and the resulting samples were centrifuged (1,900 x g for 30 minutes) and stored in the same way as the FPA samples.

Analysis of Samples
Routine hematologic variables were determined using a Technicon H.2 analyzer (Technicon Instruments, Tarrytown, NY). The plasma hemoglobin level was quantified in a Hitachi U-2000 spectrophotometer (Noka Works Hitachi, Tokyo, Japan) according to a previously described method [9] (reference value, <0.02 g/dL). The C3 activation product C3bc was measured in a double-antibody enzyme immunoassay using the monoclonal antibody bH6 reacting with a neoepitope expressed in C3b, iC3b, and C3c, but not in native C3, as the capture antibody [10]. A zymosan-activated human serumpool (n = 80), specified to contain 1,000 arbitrary units (AU)/mL of C3bc, was used as the standard (reference range, 11–21 AU/mL). The TCC was quantified in a similar double-antibody enzyme immunoassay using the monoclonal antibody aE11 specific for a C9 neoepitope expressed in TCC, but not in the native C9, as the capture antibody [11] (reference range, 2.2–6.6 AU/mL). The standard was the same as the one described for the C3bc assay. Vitronectin (S-protein) was also quantified in a double-antibody enzyme immunoassay [12]. The coating antibody was a monoclonal antibody to vitronectin, and the secondary antibody was a rabbit polyclonal antibody to vitronectin produced in our own laboratory (reference range, 0.24–0.53 g/L). Fibrinopeptide A was quantified in a modified radioimmunoassay (IMCO, Stockholm, Sweden) [13] (reference value, 1.3 ± 0.9 [SD] ng/mL). Lactoferrin was quantified in a radioimmunoassay as described [14] (reference value, 385 ± 153 [SD] x 10^-6 g/L). ß-Thromboglobulin was quantified in an enzyme immunoassay (Diagnostica Stago EIA kit Asserachrom ß-TG; Boehringer Mannheim) [13] (reference value, 27.9 ± 11.2 [SD] ng/mL).

Statistical Methods
Nonparametric analysis was used because of the small size of the groups. Intergroup comparisons were based on the sum of median values in each group, or between peak values when appropriate (Kruskal-Wallis test) [15]. The Friedman test was used to identify time-dependent changes within groups. Results are presented as median values and interquartile ranges. A p value less than 0.05 was regarded as significant.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The age distribution did not differ among the four patient groups, and although female patients were underrepresented, the male-female ratio was similar for the four groups. The number of distal anastomoses, the extracorporeal circulation time, the aortic cross-clamp time, the median ACT, the median protamine dosage, and the postoperative blood loss did not differ among the groups (Table 1).

View larger version (23K): [in this window] [in a new window]   Fig 1. . Median concentrations with interquartile range of plasma hemoglobin in patients undergoing coronary artery bypass grafting (n = 40), comparing the level in those in whom the Biomedicus centrifugal pump was used with the level in those in whom the Gambro roller pump was used, and also comparing the Carmeda BioActive Surface with the uncoated CPB surface, for a total of four groups (n = 10 in each group): centrifugal pump, uncoated (CU); centrifugal pump, coated (CC); roller pump, uncoated (RU); and roller pump, coated (RC). The plasma was sampled at the start of cardiopulmonary bypass (CPB), after 30 minutes, 10 minutes after release of the aortic cross-clamp (post ACC), 10 minutes after protamine administration, at skin closure, and 6 hours postoperatively (PO).

View larger version (26K): [in this window] [in a new window]   Fig 2. . Median plasma concentrations with the interquartile range of the C3 complement activation products C3b, iC3b, and C3c (C3bc), the terminal complement complex SC5b-9 (TCC), and the complement lytic inhibitor vitronectin in groups of patients undergoing coronary artery bypass grafting, as defined in the legend for Figure 1. (AU = arbitrary units; other abbreviations are as in Figure 1.)

Vitronectin
The vitronectin concentration decreased from the value at the start of CPB to reach minimum values of about 50% of the initial concentrations after 30 minutes on CPB in the roller pump groups and 10 minutes after release of the aortic cross-clamp in the centrifugal pump groups (see Fig 2). The initial concentration was not reestablished 6 hours postoperatively. In all four groups the minimum vitronectin concentration was significantly lower than the level at the start of CPB. The lowest concentration of vitronectin was observed in the centrifugal pump, coated group, but the minimum values did not differ significantly among the groups, and the decrease in the concentrations was similar for all groups. No significant differences in the vitronectin concentration were observed between the pump groups or between the heparin-coated and uncoated groups.

Fibrinopeptide A
The FPA concentration increased from the value at the start of CPB to reach maximum values at skin closure in all four groups (Fig 3). The maximum values were significantly higher than the baseline concentrations in all four groups (p < 0.05). The groups did not differ significantly with respect to the sum of the measurements of FPA.

View larger version (28K): [in this window] [in a new window]   Fig 3. . Median plasma concentrations with the interquartile range of fibrinopeptide A and ß-thromboglobulin in groups of patients undergoing coronary artery bypass grafting, as defined in the legend for Figure 1. (See Figure 1 for abbreviations.)

Lactoferrin
The lactoferrin concentration was almost unchanged in both the coated groups, and it was significantly increased in the two uncoated groups (Fig 4). The highest lactoferrin concentrations were measured 10 minutes after release of the aortic cross-clamp in the two uncoated groups. In the roller pump, uncoated group, the highest lactoferrin concentration was significantly higher (p = 0.03) and the sum of concentrations significantly higher (p = 0.006) than those in the roller pump, coated group. In the centrifugal pump, uncoated group, the highest lactoferrin concentration was significantly higher (p = 0.006) and the sum of concentrations significantly higher (p = 0.008) than those in the centrifugal pump, coated group. The lactoferrin concentration did not differ between the two pump groups.

View larger version (23K): [in this window] [in a new window]   Fig 4. . Median plasma concentrations with the interquartile range of lactoferrin in groups of patients undergoing coronary artery bypass grafting, as defined in the legend for Figure 1. (See Figure 1 for abbreviations.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

The increased plasma hemoglobin concentrations observed in the roller pump groups indicate hemolysis is increased in these as opposed to the centrifugal pump groups. Increased red blood cell destruction gives rise to an increased plasma hemoglobin concentration, which results in hemoglobin-haptoglobin complexes that are quickly removed by hepatocytes. Hemolysis during CPB may result from different mechanisms, but mechanical destruction of the red blood cells is probably of major importance [16]. The extent to which factors other than mechanical factors contribute to hemolysis during CPB remains uncertain. Based on findings from an in vitro study, it has previously been suggested that mechanically damaged erythrocytes are more prone to complement lysis [17]. The importance of heparin coating was observed also in the present study, because the TCC concentration was significantly reduced in the heparin-coated group irrespective of the pump type. The amount of circulating TCC should reflect the extent of complement "bystander lytic attack" on cells [18]. The adhesive protein vitronectin is an important inhibitor of bystander lysis [19–21]. In the present study we found about a 50% reduction in the vitronectin level during CPB. However, we could not demonstrate a significant effect on the vitronectin decrease attributable to the pump type.

The two pumps did not operate differently in terms of coagulation activation, nor did the heparin coating in the present study cause the FPA concentrations to be reduced. This corresponds with our in vitro findings [17]. In this context it should be pointed out that in the present study, the systemically administered heparin doses were similar for all four groups, leading to similarly prolonged ACTs in all groups (see Table 1). Thus, the major anticoagulant effect appeared to be related to the systemically administered heparin. It has been demonstrated that blood coagulation activation occurs during CPB despite intense anticoagulation with heparin [22]. On the other hand, it has previously been shown that end-point–immobilized, unfractionated heparin will adsorb factor XII [23], inhibit factor Xa through its interaction with antithrombin [23], and thus lead to less thrombin formation on surfaces coated by this technique. On the basis of these findings it appears that the net anticoagulant effect during CPB is dependent on the concentrations of immobilized heparin as well as on the amount of systemically administered heparin, the latter overshadowing the former when intense. It may be debated whether the use of full versus reduced systemic heparinization is preferable in evaluations of the biocompatibility of entirely heparin coated CPB circuits. In some previous studies [8, 24], the combination of heparin coating and reduced systemic heparinization has been found to significantly reduce granulocyte activation, compared with the granulocyte activation seen for uncoated circuits and full heparinization. The use of similar systemic heparinization in both the heparin-coated and uncoated groups probably confers an advantage for the evaluation of the heparin-coated circuits in the present study.

Our comparison of centrifugal and roller pumps in the presence and absence of entirely heparin coated surfaces in the CPB circuit was especially useful for the evaluation of platelet activation. Previous studies have indicated platelet activation is reduced when centrifugal pumps are used during open heart operations [4, 5]. The ß-TG concentration was significantly higher in the roller pump, uncoated group than in the centrifugal pump, uncoated group, but the difference was not significant when the coated groups were included in the comparison. On the basis of the findings in the present study, heparin coating may have a much greater influence on platelet activation than the pump type.

The mechanisms for platelet activation during CPB are not clear [7]. The observed differences cannot be explained by differences in the exposure time to the foreign surface, as the CPB time was similar for the four groups. If the roller pump more than the centrifugal pump results in mechanically induced activation or destruction of the platelets, this may explain the observed differences between the uncoated groups. It should be pointed out, however, that complement activates platelets, and possibly the reduced complement activation in the heparin-coated groups may contribute to the reduced release of ß-TG. Our finding that the ß-TG levels were significantly lower in the roller pump, coated group than in the roller pump, uncoated group indicates that mechanically activated platelets may be more prone to complement attacks.

The reduced lactoferrin concentrations observed in the heparin-coated versus the uncoated groups reflects reduced granulocyte activation, as previously documented both in vivo [8, 24] and in vitro [17]. There was no difference between the roller and centrifugal pump groups with respect to this granulocyte activation variable. Blood activation products, generated during CPB, may exert several effects in vivo through their interactions with various cell types and through complex amplification systems.

Our study findings indicate that the centrifugal pump causes less hemolysis (plasma hemoglobin concentration) than the roller pump and that heparin coating reduces complement activation (TCC), granulocyte activation (lactoferrin), and platelet activation (ß-TG). They also indicate that the combined use of a totally heparin coated CPB surface and a centrifugal pump can lead to improved blood compatibility during heart operations.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
We greatly appreciate the excellent technical assistance provided by the staff at the participating laboratories. The study was financially supported by grants from The Norwegian Council on Cardiovascular Disease.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Address reprint requests to Dr Moen, Department of Cardiothoracic Surgery, Ullevål University Hospital, N-0407 Oslo, Norway.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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