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Eur J Cardiothorac Surg 2002;22:527-533
© 2002 Elsevier Science NL
a Department of Cardiac Surgery, Fondation Hôpital Saint Joseph, 185 rue Raymond Losserand, 75 674 Paris Cedex 14, France
b Department of Biochemistry, Fondation Hôpital Saint Joseph, 185 rue Raymond Losserand, 75 674 Paris Cedex 14, France
Received 18 September 2001; received in revised form 9 April 2002; accepted 14 June 2002.
* Corresponding author. Tel.: +33-144-123-376; fax: +33-144-123-682
e-mail: y.fromes{at}myologie.chups.jussieu.fr
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Abstract |
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 Top Abstract 1. Introduction2. Methods and materials3. Results4. DiscussionAppendix A. Conference...References |
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), as well as neutrophil elastase secretion and ß-thromboglobulin release from platelets and S100 protein assay were performed. Serial blood samples were taken prior to the onset, after initiation, at the end and after weaning of the CPB; further samples were collected 6 and 24 h after the end of the CPB. Results: All patients were similar with regards to pre- and intra-operative characteristics and clinical outcomes were comparable for both groups. MECC system allowed a reduced hemodilution with a mean drop of the hematocrit of 8.5 vs. 15.3% (P<0.05). Mononuclear phagocytes dropped in a more important manner under standard CPB conditions (247±151 vs. 419±168, P=0.002), but both groups demonstrated a rise in monocyte count at the end of the CBP. No significant release of IL-1ß was observed in either group. By the end of CPB, IL-6 levels were significantly lower in the MECC group (38.8±19.6 vs. 87.9±78.9, P=0.04), despite a higher monocyte count. Plasma levels of TNF- rised significantly more during standard CPB than with the MECC system (17.8±15.4 vs. 10.1±5.6, P=0.002). With MECC, the neutrophil elastase release was reduced (72.7±47.9 vs. 219.6±103.4, P=0.001). Platelet count remained at higher values with the minimal compared to standard CPB. It is noteworthy to consider that ß-thromboglobulin levels showed slightly lower platelet activation in the MECC group at all times of CPB (110.5±55.6 vs. 134.7±46.8, P=0.10). The pattern of release of S100 protein showed higher values in patients undergoing standard CPB than after MECC. Conclusions: The MECC system is suitable to maintain total extracorporeal circulation and demonstrates a lower inflammatory reaction when compared to standard CPB.
Key Words: Coronary artery bypass grafting • Extracorporeal circulation • Inflammation • Cytokines • S100 protein
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1. Introduction |
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TopAbstract1. Introduction2. Methods and materials3. Results4. DiscussionAppendix A. Conference...References |
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The inflammatory response is initiated by a large number of processes that act on both the cellular and humoral elements of blood. Some cytokines, such as interleukin-1 (IL-1ß), interleukin-6 (IL-6) or tumor necrosis factor (TNF-) that can be stimulated by a broad spectrum of stimuli, are able to act on a large number of effectors [5,6]. Thus, they may reflect the status of the inflammatory response in the situation where multiple initiating processes are involved. Cytokines appear to mediate a large number of cellular events that contribute to the injurious processes after bypass. Leukocytes are the central cell type in the inflammatory response; their recruitment, activation and cytotoxic effects contribute largely to the damaging process. The pathophysiologic responses that are responsible for the systemic inflammatory reaction may continue long after the discontinuation of the bypass [7]. Regarding the local inflammatory reactions at the level of the myocardium, which are mainly due to the mechanisms of ischemia and reperfusion, CPB may contribute to the extent of the injuries [8]. The reduced release of pro-inflammatory cytokines may play an important role in limiting the postoperative inflammatory response syndrome.
So, lessening the invasive aspects in coronary surgery is of constant concern. As CPBs are known to cause part of the systemic inflammatory reaction that can be responsible for significant morbidity and mortality, off-pump CABG can be one solution to this problem, however, CPB will still be needed for many procedures in cardiac surgery. Even without considering open-heart surgery, it is noteworthy to consider the hemodynamic benefit of the control of cardiac output by CPBs during CABG procedures. Using the current CPB techniques, CABG operations have reached a level of excellence that sets the hallmark to which new techniques have to be compared. A novel technique based on a minimal extra corporeal circulation (MECC) system is able to provide this hemodynamic stability, combined with a extensive biocompatibility given by the complete coating of the CBP system, lines and cannulae [9]. The present work aimed to evaluate the MECC® with regard to the inflammatory response in a prospective study involving patients undergoing CABG. Several humoral parameters, such as cytokine secretion, and also the cellular responses were investigated. This study suggests strongly that besides the excellent hemodynamic outcomes, a significant reduction of the inflammatory reaction can be observed, making the MECC® system an attractive solution for minimally invasive CPBs.
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2. Methods and materials |
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TopAbstract1. Introduction2. Methods and materials3. Results4. DiscussionAppendix A. Conference...References |
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For standard CPB, a membrane oxygenator with a cardiotomy reservoir was used with a roller pump (Stoeckert, France) at a non-pulsatile flow of 2.6 l/min m2. The MECC system consists of a closed system associating a Rotaflow® centrifugal pump (Jostra, France) and a Quadrox® membrane oxygenator (Jostra, France). Fundamental components are reduced to the minimal elements, including short arterial and venous lines. The venous line is directly connected to the pump head. Suppression of the open venous reservoir eliminates the blood–air interface and allows reduced priming volumes. No aortic venting was used during this set-up. All lines and cannulae were treated with the Bioline® coating (Jostra, France). All patients received 300 UI/kg bovine heparin infused intravenously before onset of CPB, and anticoagulation was monitored by measuring activated clotting time with a hemochron system. At the end of CPB, intravenous application of protamine sulfate in a 1:1 ratio of the initial dose of heparin served to antagonize heparin effects. Blood from the surgical field was mainly (for the standard CPB) or exclusively (for the MECC system) collected in a cell saving device. After skin closure the blood was centrifuged, washed in Ringer's lactate solution, recentrifuged and returned to the patient. No homologous blood products were used in either group of patients.
CABG operations were performed under total aortic cross-clamping. Warm blood cardioplegia was delivered intermittently by an antegrade route in both groups and the MECC system did not interfere with the quality of the myocardial protection, as controlled by the cardiac troponin I (cTn I) release.
Besides routine clinical and biochemical investigations, specific evaluation of cytokine release (IL-1ß, IL-6 and TNF-) was performed. Enzyme-linked immunosorbant assay (ELISA) assays were used with a minimum detectable dose of 5.0 pg/ml, respectively (Amersham).
Moreover, the release of neutrophil elastase as well as platelet activation by serial dosage of ß-thromboglobulin, were investigated using an ELISA immunoassay kit with lower detection limit of 2.0 ng/ml (Immunotech).
S100B protein was measured by an ELISA method using a commercial kit, with a detection limit of less than 0.20 pg/ml (Sangtec 100, Byk-Sangtec Diagnostica).
Serial blood samples were taken prior to the onset (T1), after initiation (T2), at the end (T3) and after weaning of the CPB (T4); further samples were collected 6 (T5) and 24 h (T6) after the end of the CPB.
2.1. Statistics
Continuous data are presented as mean±SD. Unpaired Student's t-test was used for analysis with the assumption of a normal distribution. Further analysis was carried out using a distribution-free test, Mann–Whitney U-test. A P value of <0.05 was considered a statistically significant difference. Analyses were performed using Statview software (SAS Institute, Inc.).
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3. Results |
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TopAbstract1. Introduction2. Methods and materials3. Results4. DiscussionAppendix A. Conference...References |
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3.2. Hematologic parameters and inflammatory cytokines
Mononuclear phagocytes dropped in a more important manner during CPB under standard CPB conditions, reaching a lowest level by the end of the bypass period (247±151 vs. 419±168, P=0.002), but both groups demonstrated a rise in monocyte count during the first 24 h after CPB. Thus, the rise of monocytes was more important in the standard CPB group (Fig. 1
).
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The time course of IL-6 release in peripheral blood shows a peak after termination of CPB. In the MECC group, IL-6 levels were significantly lower (38.8±19.6 vs. 87.9±78.9, P=0.04). The IL-6 release should at least in part be compared to the higher monocyte count at the same time point (Fig. 1).
Plasma levels of TNF- rose significantly during standard CPB. The increase was faster and greater in this group, reaching a peak value by the end of the bypass. Even if an increase of TNF- was observed when the MECC system was used, the extent of the rise was significantly lower with this new technique (17.8±15.4 vs. 10.1±5.6, P=0.002) (Fig. 2
).
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4. Discussion |
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TopAbstract1. Introduction2. Methods and materials3. Results4. DiscussionAppendix A. Conference...References |
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However, extracorporeal circulation exposes the entire blood mass to biomaterials in the perfusion circuit and to non-endothelial cells in the wound. Normally, blood cells and proteins interface only with the endothelium and endothelial cells accomplish a complex protective role towards the blood constituents. Contact of the blood with foreign surfaces during CPB triggers defense reactions, which have a broad spectrum of actions throughout the whole body. In particular, extracorporeal circulation is not possible without anticoagulation and heparin remains the most commonly used anticoagulant. Heparin can be bound to certain biomaterials in order to increase the biocompatibility. Even if the clinical benefits might be difficult to document, because the surface properties are not similar to those of endothelial cells, the heparin coating might contribute to decrease the thrombin formation and attenuate the inflammatory response [4,9–11].
Recently, a minimized extracorporeal circulation (MECC) system has been developed based on the concept of a short closed total CPB circuit. The basic elements are formed by a centrifugal pump, a membrane oxygenator and an arterial filter. The priming volume could be reduced to 500 ml or less, thus limiting the hemodilution. The complete circuit is heparin-coated in order to maximize the biocompatibility. Blood–air interface is eliminated and suction of shed blood is operated only through a cell saving device. Thus, blood is washed prior to retransfusion into the patient.
The present study confirms the excellent clinical results of the new technique, but the main goal was to analyze the inflammatory reaction with reference to standard CPB.
Myocardial protection was carried out by hyperkaliemic warm blood cardioplegia, which was administered intermittently by an antegrade route. This technique ensures excellent myocardial protection, as shown previously [12]. Despite the small bypass volume, the MECC system is compatible with this kind of cardioplegia. In fact, all patients underwent the same type of cardioplegia and no significant differences could be observed concerning cardiac adverse events. Routinely, myocardial preservation was checked by serial sampling for blood levels of cardiac tropinin I, a highly sensitive marker for myocardial injuries.
Leukocytes are known to be major actors in the inflammatory reaction after bypass [13]. Serum interleukins (IL-1ß, IL6) are considered as markers for systemic inflammation [13]. However, conflicting results exist on the IL-1ß response, which remained undetectable in some studies, whereas others measured significant plasma levels [7,14,15]. Our data support the idea that there is no significant release of IL-1ß during the bypass and the early postoperative period. So far, CPB should not be considered as stimulating the IL-1ß secretion in the blood stream. However, given the complex biological secretion pathway of this interleukin, we cannot eliminate the stimulation of IL-1ß synthesis and intracellular storage, which could lead to secondary release under different bypass conditions. IL-6 is a proinflammatory cytokine with plasma concentrations that have been noted to increase in response to many major surgeries, as well as after cardiac surgery with CPB. IL-6 is a pleiotropic molecule with multiple biological activities and direct inotropic negative effects. The sources of IL-6 are uncertain, but mononuclear macrophages are able to release this cytokine among others. Thus, plasma levels of IL-6 should be considered with regard to the monocyte count. Despite the fact that mononuclear phagocytes fall to lower levels in the control group, higher levels of several cytokines were observed during CPB in the control group. The MECC system seems to trigger a lower activation of monocytes, leading to a lesser release of IL-6.
TNF- is a potent proinflammatory cytokine with negative inotropic properties [16]. This cytokine is elaborated in many pathological situations, as shock, acute myocarditis, heart failure and ischemia/reperfusion injuries [15]. The release of TNF- has been associated with the development of complications after CPB. The origin of TNF- was not clearly determined. Under certain conditions of stress, the heart is able to synthesize biologically active TNF-, whereas there is no evidence for the biosynthesis of TNF- in non-failing hearts [16]. In our study, myocardial preservation with reference to cardiac troponin I, was equally effective in both groups. So far, plasma levels of TNF- may not be related to differences in myocardial protection, but rather to the type of bypass used during surgery.
Neutrophils respond to soluble inflammatory mediators not only by phagocytosing foreign pathogens and damaged tissue particles, but also by releasing toxic substances and proinflammatory mediators recruiting more leukocytes. Among the substances of activated neutrophils release, elastase appears to have the capacity to mediate multiple actions that facilitate the inflammatory process [17–19]. The time course of elastase release during and after CPB shows a significant decrease in stimulation when the MECC system is used. Lower systemic cytokine release rates might explain part of this beneficial effect, which is correlated with lower levels of elastase release. Thus, the MECC system might represent an attractive alternative to off-pump cardiac surgery as far as the inflammatory reaction is concerned.
The ß-thromboglobulins are among the major chemokines released by platelets [20]. The time course of the platelet release reaction was followed during the bypass and the MECC group revealed lower levels of ß-thromboglobulin, despite higher platelet counts. After weaning from the CPB and during the early postoperative period platelet count and ß-thromboglobulin levels did not display a significantly different evolution. It might be noteworthy to point out that both groups of patients were submitted to full-dose heparin treatment and thus full-dose antagonization by protamine. This might explain the similar evolution of the platelet parameters during the initial postoperative times.
Finally, we have analyzed the S100B protein, which has been described as a serum marker to assist in the diagnosis of cerebral injuries after CPB [21]. Several authors have indicated the usefulness of S100B protein as an early marker for brain damage. Our study shows a significantly lower release of this protein into the peripheral blood when the MECC system was used. No clinically relevant neurological event was observed during this study. However, these positive results should not be considered as reflecting solely the absence of brain damage, as it has been shown recently, that most serum S100B may be of extra-cerebral origin [22–25]. The exclusive use of a cell saving device to treat the shed blood could largely be explained by the decrease of serum levels in S100B and the avoidance of the artificial increase of S100B. Thus, the diagnostic value of S100B protein for brain damage at distance of the surgical procedure might be preserved.
In summary, the MECC system demonstrates good evidence for a lower inflammatory reaction when compared to standard CPB. It is clear that IL-6, TNF- and elastase release are significantly more limited for those patients when the MECC system was used. As TNF- appears to exert direct negative inotropic effects, this point might be of crucial importance in patients with poor cardiac condition, which will be a risk considering the hemodynamic instability during the surgical procedure. Thus, the MECC system may provide a minimally invasive solution to maintain the high surgical standards of CABG surgery with CPB and it may avoid many of the deleterious effects of standard CPB methods.
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Footnotes |
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Appendix A. Conference discussion |
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TopAbstract1. Introduction2. Methods and materials3. Results4. DiscussionAppendix A. Conference...References |
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Dr Fromes: Well, let me answer you in two times. Yes, there is a limited hemodilution, and in the cases of the MECC we have about an 8% loss of hematocrit, meaning that there is roughly a reduction of 50% of the hemodilution in our cases. A decreased need for blood transfusion, none of the patients were transfused in our study. That was one of the criteria, to study more effectively the inflammation. So it might be difficult to answer that there is really a reduction in this case. But generally speaking, our experience with the MECC system means that there is a reduction of blood transfusion, yes, correct.
Dr Diena: What about the suction of the aortic vent and the suction on the fill?
Dr Fromes: In this case, in the study group, there was no aortic venting, but there shouldn't be any problem in adding a venting system and to bring it back to the membrane.
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References |
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TopAbstract1. Introduction2. Methods and materials3. Results4. DiscussionAppendix A. Conference...References |
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and tumor necrosis factor receptors in the failing human heart. Circulation 1996;93:704-711.This article has been cited by other articles:
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C. A. Skrabal, Y. H. Choi, A. Kaminski, M. Steiner, G. Kundt, G. Steinhoff, and A. Liebold Circulating endothelial cells demonstrate an attenuation of endothelial damage by minimizing the extracorporeal circulation. J. Thorac. Cardiovasc. Surg., August 1, 2006; 132(2): 291 - 296. [Abstract] [Full Text] [PDF]
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I. Deblier, A. M. Sadowska, A. Janssens, I. Rodrigus, and W. A. DeBacker Markers of inflammation and oxidative stress in patients undergoing CABG with CPB with and without ventilation of the lungs: a pilot study Interactive CardioVascular and Thoracic Surgery, August 1, 2006; 5(4): 387 - 391. [Abstract] [Full Text] [PDF]
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E. Hickey, T. Karamlou, J. You, and R. M. Ungerleider Effects of Circuit Miniaturization in Reducing Inflammatory Response to Infant Cardiopulmonary Bypass by Elimination of Allogeneic Blood Products Ann. Thorac. Surg., June 1, 2006; 81(6): S2367 - S2372. [Abstract] [Full Text] [PDF]
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O. M. Bical, Y. Fromes, D. Gaillard, M. Fischer, O. Ponzio, P. Deleuze, M.-F. Gerhardt, and F. Trivin Comparison of the inflammatory response between miniaturized and standard CPB circuits in aortic valve surgery. Eur. J. Cardiothorac. Surg., May 1, 2006; 29(5): 699 - 702. [Abstract] [Full Text] [PDF]
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K. Wiebe, H. Baraki, P. Macchiarini, and A. Haverich Extended pulmonary resections of advanced thoracic malignancies with support of cardiopulmonary bypass Eur. J. Cardiothorac. Surg., April 1, 2006; 29(4): 571 - 577. [Abstract] [Full Text] [PDF]
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C. Beghi, F. Nicolini, A. Agostinelli, B. Borrello, A. M. Budillon, F. Bacciottini, M. Friggeri, A. Costa, L. Belli, L. Battistelli, et al. Mini-Cardiopulmonary Bypass System: Results of a Prospective Randomized Study Ann. Thorac. Surg., April 1, 2006; 81(4): 1396 - 1400. [Abstract] [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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A. Liebold, A. Khosravi, B. Westphal, C. Skrabal, Y.H. Choi, C. Stamm, A. Kaminski, A. Alms, T. Birken, D. Zurakowski, et al. Effect of closed minimized cardiopulmonary bypass on cerebral tissue oxygenation and microembolization J. Thorac. Cardiovasc. Surg., February 1, 2006; 131(2): 268 - 276. [Abstract] [Full Text] [PDF]
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 S. Rex, S. Brose, S. Metzelder, L. de Rossi, S. Schroth, R. Autschbach, R. Rossaint, and W. Buhre Normothermic Beating Heart Surgery with Assistance of Miniaturized Bypass Systems: The Effects on Intraoperative Hemodynamics and Inflammatory Response Anesth. Analg., February 1, 2006; 102(2): 352 - 362. [Abstract] [Full Text] [PDF]
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G. Nollert, I. Schwabenland, D. Maktav, F. Kur, F. Christ, P. Fraunberger, B. Reichart, and C. Vicol Miniaturized Cardiopulmonary Bypass in Coronary Artery Bypass Surgery: Marginal Impact on Inflammation and Coagulation but Loss of Safety Margins Ann. Thorac. Surg., December 1, 2005; 80(6): 2326 - 2332. [Abstract] [Full Text] [PDF]
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S. G Raja and G. D Dreyfus Modulation of Systemic Inflammatory Response after Cardiac Surgery Asian Cardiovasc Thorac Ann, December 1, 2005; 13(4): 382 - 395. [Abstract] [Full Text] [PDF]
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S. Dial, E. Delabays, M. Albert, A. Gonzalez, J. Camarda, A. Law, and D. Menzies Hemodilution and surgical hemostasis contribute significantly to transfusion requirements in patients undergoing coronary artery bypass J. Thorac. Cardiovasc. Surg., September 1, 2005; 130(3): 654 - 654. [Abstract] [Full Text] [PDF]
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A. Koster, W. Bottcher, F. Merkel, R. Hetzer, and H. Kuppe The more closed the bypass system the better: a pilot study on the effects of reduction of cardiotomy suction and passive venting on hemostatic activation during on-pump coronary artery bypass grafting Perfusion, September 1, 2005; 20(5): 285 - 288. [Abstract] [PDF]
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U. Abdel-Rahman, F. Ozaslan, P. S. Risteski, S. Martens, A. Moritz, A. Al Daraghmeh, H. Keller, and G. Wimmer-Greinecker Initial Experience With a Minimized Extracorporeal Bypass System: Is There a Clinical Benefit? Ann. Thorac. Surg., July 1, 2005; 80(1): 238 - 243. [Abstract] [Full Text] [PDF]
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J. Wippermann, J. M. Albes, M. Hartrumpf, M. Kaluza, R. Vollandt, R. Bruhin, and T. Wahlers Comparison of minimally invasive closed circuit extracorporeal circulation with conventional cardiopulmonary bypass and with off-pump technique in CABG patients: selected parameters of coagulation and inflammatory system Eur. J. Cardiothorac. Surg., July 1, 2005; 28(1): 127 - 132. [Abstract] [Full Text] [PDF]
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 W.-J. P. van Boven, W. B. M. Gerritsen, P. Zanen, J. C. Grutters, H. P. A. van Dongen, A. Bernard, and L. P. H. J. Aarts Pneumoproteins as a Lung-Specific Biomarker of Alveolar Permeability in Conventional On-pump Coronary Artery Bypass Graft Surgery vs Mini-Extracorporeal Circuit: A Pilot Study Chest, April 1, 2005; 127(4): 1190 - 1195. [Abstract] [Full Text] [PDF]
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H. Takai, K. Eishi, S. Yamachika, S. Hazama, T. Ariyoshi, and K. Nishi Demonstration and Operative Influence of Low Prime Volume Closed Pump Asian Cardiovasc Thorac Ann, March 1, 2005; 13(1): 65 - 69. [Abstract] [Full Text] [PDF]
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M A. Huybregts, R de Vroege, H M. Christiaans, A L Smith, and R C. Paulus The use of a mini bypass system (Cobe Synergy) without venous and cardiotomy reservoir in a mitral valve repair: a case report Perfusion, March 1, 2005; 20(2): 121 - 124. [Abstract] [PDF]
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S. W Sutton, M. A Duncan, V. A Chase, B. L Hamman, and E. H Cheung Perfusion-assisted beating heart support with a miniature extracorporeal circuit and leukocyte filtration: a 58-year-old patient with severe COPD Perfusion, December 1, 2004; 19(6): 369 - 373. [Abstract] [PDF]
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M. Ando, Y. Takahashi, and N. Suzuki Open Heart Surgery for Small Children Without Homologous Blood Transfusion by Using Remote Pump Head System Ann. Thorac. Surg., November 1, 2004; 78(5): 1717 - 1722. [Abstract] [Full Text] [PDF]
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J.P. Remadi, Z. Rakotoarivello, P. Marticho, F. Trojette, A. Benamar, H. Poulain, and C. Tribouilloy Aortic valve replacement with the minimal extracorporeal circulation (Jostra MECC System) versus standard cardiopulmonary bypass: A randomized prospective trial J. Thorac. Cardiovasc. Surg., September 1, 2004; 128(3): 436 - 441. [Abstract] [Full Text] [PDF]
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R de Vroege, F te Meerman, L Eijsman, W R Wildevuur, C. R. Wildevuur, and W van Oeveren Induction and detection of disturbed homeostasis in cardiopulmonary bypass Perfusion, September 1, 2004; 19(5): 267 - 276. [Abstract] [PDF]
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W J van Boven, W B Gerritsen, F G Waanders, F J Haas, and L P Aarts Mini extracorporeal circuit for coronary artery bypass grafting: initial clinical and biochemical results: A comparison with conventional and off-pump coronary artery bypass grafts concerning global oxidative stress and alveolar function Perfusion, July 1, 2004; 19(4): 239 - 246. [Abstract] [PDF]
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J.-P. Remadi, P. Marticho, I. Butoi, Z. Rakotoarivelo, F. Trojette, A. Benamar, S. Beloucif, D. Foure, and H. J. Poulain Clinical experience with the mini-extracorporeal circulation system: an evolution or a revolution? Ann. Thorac. Surg., June 1, 2004; 77(6): 2172 - 2175. [Abstract] [Full Text] [PDF]
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D. L. Ngaage Off-pump coronary artery bypass grafting: the myth, the logic and the science Eur. J. Cardiothorac. Surg., October 1, 2003; 24(4): 557 - 570. [Abstract] [Full Text] [PDF]
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T Gourlay and P Connolly Does cardiopulmonary bypass still represent a good investment? The biomaterials perspective Perfusion, July 1, 2003; 18(4): 225 - 231. [Abstract] [PDF]
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T. Gourlay, I. Samartzis, and K. M Taylor The effect of haemodilution on blood/biomaterial contact-mediated CD11b expression on neutrophils: ex vivo studies Perfusion, March 1, 2003; 18(2): 87 - 93. [Abstract] [PDF]
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