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Ann Thorac Surg 2000;69:1198-1204
© 2000 The Society of Thoracic Surgeons

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ORIGINAL ARTICLES: CARDIOVASCULAR

Inflammatory response after coronary revascularization with or without cardiopulmonary bypass

^a Bristol Heart Institute, Bristol Royal Infirmary, Bristol, United Kingdom

Address reprint requests to Dr Angelini, Bristol Heart Institute, Bristol Royal Infirmary, Bristol, BS2 8HW, United Kingdom
e-mail: g.d.angelini{at}bristol.ac.uk

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. We sought to investigate the effect of multiple coronary artery bypass grafting (CABG) with or without cardiopulmonary bypass (CPB) on the perioperative inflammatory response.

Methods. Sixty patients undergoing CABG were randomly assigned to one of two groups: (A) on pump with conventional CPB and cardioplegic arrest, and (B) off pump on the beating heart. Serum samples were collected for estimation of neutrophil elastase, interleukin 8 (IL-8), C3a, and C5a preoperatively and at 1, 4, 12, and 24 hours postoperatively. Furthermore, white blood cell (WBC), neutrophil, and monocyte counts were carried out preoperatively and at 1, 12, 36 and 60 hours postoperatively. Overall incidence of infection and perioperative clinical outcome were also recorded.

Results. The groups were similar in terms of age, weight, gender ratio, extent of coronary disease, left ventricular function, and number of grafts per patient. Neutrophil elastase concentration peaked early after CPB in the on-pump group, with a decline with time. Repeated-measures analysis of variance between groups and comparisons at each time point (modified Bonferroni) showed elastase concentrations were significantly higher in the on-pump than the off-pump group (both p < 0.0001). IL-8 increased significantly after surgery in the on-pump group, with no decline during the observation period (p = 0.01 vs off pump). C3a and C5a rose early after surgery in both groups when compared with baseline values. Postoperative WBC, neutrophil, and monocyte counts were significantly higher in the on-pump than the off-pump group (p < 0.01). Finally, the incidence of postoperative overall infections was significantly higher in the on-pump group (p < 0.0001 vs off pump).

Conclusions. CABG on the beating heart is associated with a significant reduction in inflammatory response and postoperative infection when compared with conventional revascularization with CPB and cardioplegic arrest.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Despite advances in perfusion, anesthetic, and surgical techniques, cardiopulmonary bypass (CPB) is still reported to evoke inflammatory reactions that may lead to postoperative morbidity such as bleeding, thromboembolism, fluid retention, and temporary organ dysfunction [1–6].

Prevention of the CPB-mediated inflammatory response (IR) has been attempted using different techniques of perfusion and pharmacological agents, but with little success [7, 8]. Many centers now perform coronary artery bypass grafting (CABG) on the beating heart without CPB, thus avoiding the CPB-mediated IR [9–11]. However, recent studies that have investigated CABG with or without CPB as a determinant of IR report a contradictory outcome [12, 13]. Furthermore, there has been no prospective randomized study assessing the role of conventional and beating heart surgery on the perioperative IR.

The aim of this prospective randomized study was to investigate the effect of CABG with or without CPB on the IR. A variety of surrogate markers of the IR were used to determine the magnitude and temporal nature of this response.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Patient selection
Sixty patients (48 males, mean age 60.9 ± 9.1 years) undergoing first-time CABG were enrolled in the study. Patients were prospectively randomized into two groups by card allocation. Group A (on pump) underwent conventional myocardial revascularization with CPB and cardioplegic arrest of the heart, whereas group B (off pump) underwent beating heart surgery. Exclusion criteria included acute infections, known immunologic diseases, impaired left ventricular function (ejection fraction of < 30%), recent myocardial infarction (< 1 month), insulin-dependent diabetes, acute or chronic renal failure, reoperation, respiratory impairment, previous stroke or transient ischemic attack, and coagulopathy. Patients with coronary disease involving branches of the circumflex artery distal to the first obtuse marginal branch and posterior branches originating from the left system were also excluded from the study, as these were felt to be technically difficult for adequate revascularization at the beginning of our experience with off-pump surgery. The rationale to exclude high-risk patients was based on the evidence that they may carry a higher possibility of IR activation [4].

The study was approved by the United Bristol Healthcare Trust Ethics Committee.

Anesthetic technique
Anesthetic technique was standardized for all patients. This consisted of intravenous anesthesia with propofol infusion at 3 mg/kg/h combined with Remifentanyl infusion at 0.5 to 1.0 µg/kg/min. Neuromuscular blockade was achieved by 0.1 to 0.15 mg/kg pancuronium bromide or vecuronium, and the lungs were ventilated to normocapnia with air and oxygen (45% to 50%) without positive end expiratory pressure (PEEP). In the on-pump group, metaraminol or phentolamine were used to maintain the systemic pressure between 50 and 60 mm Hg. In the off-pump group, mean arterial pressure of 60 mm Hg or above was maintained with increments of metaraminol 0.5 to 1.0 mg or volume as dictated by the hemodynamic condition, in combination with esmolol to maintain a heart rate below 70 beats per minute. In addition to peripheral venous lines, all patients in both groups received a central venous line and a radial artery line. Perioperative antibiotic prophylaxis consisted of flucloxacillin (1 g every 6 hours for 24 hours).

Intensive care unit management
At the end of surgery, patients were transferred to the intensive care unit (ICU). The lungs were ventilated with 60% oxygen using volume-controlled ventilation (Servo Ventilator 900C; Siemens, Stockholm, Sweden) and a tidal volume of 10 mL/kg with 5 cm H₂O of PEEP. Adjustments in FiO₂ and respiratory rate were made according to routine blood gas analysis, in order to maintain PaO₂ between 80 and 100 mm Hg, and PaCO₂ between 35 and 40 mm Hg. Forced air warming was used, until a stable nasopharyngeal temperature of 37°C had been reached. When fully warmed, patients were extubated.

Heparin and protamine management
In the on-pump group, the heparin was given at a dose of 300 IU/kg to achieve a target activated clotting time (ACT) of 480 seconds or above before commencement of CPB. The ACT was monitored during the bypass period (every 15 minutes) and an additional 3,000 IU of heparin was administered if required. In the off-pump group, heparin (100 IU/kg) was administered before the start of the first anastomosis. The target ACT in this group was of 250 to 350 seconds. Protamine was used at the end to reverse the effect of heparin and return the ACT to preoperative levels in both groups.

Surgical technique
Group A on pump
Cardiopulmonary bypass was instituted using ascending aortic cannulation and a two-stage venous cannulation in the right atrium. A standard circuit was used: a Bard tubing set, which included a 40-µm filter, a Stockert roller pump (Sorin Biomedica, Midhurst, UK), and a hollow-fiber membrane oxygenator (Monolyth; Sorin Biomedica, Midhurst, UK). The extracorporeal circuit was primed with 1,000 mL Hartmann’s solution, 500 mL Gelofusine, 0.5 g/kg Mannitol, 7 mL 10% calcium gluconate, and 60 mg heparin.

Nonpulsatile flow was used. The flow rate throughout bypass was 2.4 L/m²/min. Systemic temperature was kept between 34°C and 36°C. Myocardial protection was achieved by using intermittent anterograde hyperkalemic warm blood cardioplegia. Once completing all distal anastomoses, the aortic cross-clamp was removed and the proximal anastomosis performed with partial clamping. Corticosteroids or aprotinin were not used, as these have been reported to reduce the IR during CPB [7].

Group B off pump
The method of exposure and stabilization to perform the anastomosis was a combination of the technique previously described by our group [14], and the use of the CTS retractor (Cardiothoracic Systems Inc, Cupertino, CA). The target vessel was then exposed and snared above the chosen point for anastomosis by using a 4-0 Prolene suture with a soft plastic snugger to prevent coronary injury. The coronary artery was then opened and the anastomosis performed. Visualization was enhanced by using the surgical blower-humidifier (model SSVW-002, Surgical Site Visualization Wand; Research Medical Inc., Midvale, UT) with 1/4 PVC gas line and fluid administration set connected to a regulated gas source of medical air. An intracoronary shunt (Anastoflo Intravascular Shunt; Research Medical Inc) was used only in case of relative electrocardiographic or hemodynamic instability and excessive bleeding during the anastomosis.

Inflammatory markers, samples collection, and assay
Blood samples for inflammatory markers assay were collected from the central venous pressure (CVP) line at the following times: at the anesthetic induction, 30 minutes postcessation of CPB in the on-pump group or 30 minutes after completion of all anastomoses in the off-pump group, and thereafter at 4, 12, and 24 hours postoperatively. Samples (10 mL) were collected in bottles containing EDTA and placed immediately under ice. Each sample was then centrifuged at 1,500 g for 10 minutes and the serum was collected into small Eppendorff vials and frozen to -70°C for later batch analysis.

The following set of inflammatory mediators was chosen to evaluate the extent of the systemic inflammatory response: neutrophil elastase, interleukin 8 (IL-8), C3a, and C5a.

Neutrophil elastase is an endopeptidase that has been used as a marker of neutrophil activation [15]. IL-8 is a potent neutrophil chemotactic and activating factor [4]. Enzyme-linked immunosorbent assay (ELISA) techniques (Biotrak; Amersham Life Science, Buckinghamshire, UK) were applied to determine polymorphonuclear elastase and IL-8. Activation of the common complement pathway leads to the production of C3a and C5a. These were measured by radioimmunoassay (RIA) (Biotrak; Amersham Life Science).

White blood cell (WBC) counts, sample collection, and assay
WBC correlates with ongoing infection [6], whereas neutrophil and monocyte produce elastase and IL-8, respectively [4]. Therefore, the measurement of their levels during IR is also of utmost value. Blood samples for evaluation of WBC counts with complete differential counts were obtained before anesthetic induction and 30 minutes postcessation of CPB in the on-pump group or 30 minutes after completion of all anastomoses in the off-pump group, and thereafter at 12, 36, and 60 hours postoperatively, following our unit protocol.

Samples were drawn into 4-mL vacuum containers (Vacuette; Greiner, Labortechnik, Austria) containing potassium EDTA. These were then analyzed on an H2/H3 Technicon instrument (Bayer, Munich, Germany).

Microbiology
In the presence of persistent pyrexia, lung collapse on chest roentgenogram, clinical evidence of wound infection blood, urine, sputum, and wound swabs were taken for culture, on the judgement of the responsible physician who was blinded to the study randomization.

Postoperative morbidity
The overall incidence of infections as defined by positive culture was recorded. More specifically, chest infection was defined as positive sputum culture requiring antibiotic therapy. Wound infection was defined as the presence of discharge with positive swab culture. The duration of artificial ventilation was accepted as a gross evaluation of pulmonary function in the absence of hemodynamic instability. Clinical diagnostic criteria for perioperative myocardial infarction were new Q waves of greater than 0.04 ms, or a reduction in R waves greater than 25% in at least two leads.

Statistical analysis
Data are presented as mean ± standard deviation in tables and as mean ± standard error in figures. Comparisons between preoperative characteristics and postoperative variables were made using Fisher’s exact test or ² test where appropriate. Two-way ANOVA for repeated measurements was used to assess group differences with interaction of time and treatment effects. Bonferroni test was used for post-hoc multiple comparisons. Analyses were performed using Statview (SAS Institute Inc, Cary, NC).

	Results

Top Abstract Introduction Material and methods Results Comment References

 
The groups were similar in terms of age, body surface area, gender ratio, and extent of coronary disease, left ventricular function, and number of grafts per patient. Preoperative and intraoperative patient characteristics are shown in Table 1. No deaths, acute renal failure (ARF), or stroke occurred. One patient in the on-pump group suffered a perioperative myocardial infarction.

View larger version (11K): [in this window] [in a new window]   Fig 1. Changes in neutrophil elastase concentrations over time. Preoperative and 1, 4, 12, and 24 hours postoperative. (Filled circles) On-pump group (n = 30); (open circles) off-pump group (n = 30). p < 0.0001 on pump vs off pump.

View larger version (12K): [in this window] [in a new window]   Fig 2. Changes in IL-8 concentrations over time. Preoperative and 1, 4, 12, and 24 hours postoperative. (Filled circles) On-pump group (n = 30); (open circles) off-pump group (n = 30). p = 0.01 on pump vs off pump.

View larger version (13K): [in this window] [in a new window]   Fig 3. Changes in C3a concentrations over time. Preoperative and 1, 4, 12, and 24 hours postoperative. (Filled circles) On-pump group (n = 30); (open circles) off-pump group (n = 30). *p < 0.0001 vs baseline values; p = 0.0197 vs off pump. Comparison over time (ANOVA) did not show a significant difference.

View larger version (12K): [in this window] [in a new window]   Fig 4. Changes in C5a concentrations over time. Preoperative and 1, 4, 12, and 24 hours postoperative. (Filled circles) On-pump group (n = 30); (open circles) off-pump group (n = 30). *p = 0.0116 vs off pump. Comparison over time (ANOVA) did not show a significant difference.

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
The incidence of life-threatening morbidity and mortality after CPB has significantly decreased in recent years, however, the IR to cardiac operations is still commonly recognized and may vary in clinical significance [6]. Surgical maneuvers, contact of blood components with the artificial surface of the bypass circuit, aortic cross-clamping, and reperfusion injury are considered the main causative factors [1–3, 6, 12, 16], determined by activation of complement, macrophages, neutrophils, and cytokines [4–6]. Preventing or attenuating activation of these elements during open heart operations should offer a means of substantially reducing potential morbidity.

Several studies have already investigated the efficacy of different strategies to inhibit inflammation during conventional CABG with CPB. Heparin-coated CPB circuit [8], leukocyte depletion [7, 17], corticosteroids [7, 18], and aprotinin [1, 7] have been reported to partially attenuate CPB-mediated IR.

Multiple coronary grafting without CPB on the beating heart may reduce morbidity [9–11, 19]. Several authors have undertaken comparative studies between groups of patients undergoing CABG with or without CPB in order to identify the mechanisms of the CPB-mediated IR. However, the results of these investigations are controversial. Fransen and associates [12] reported that the acute IR in CABG patients, which has historically been ascribed to CPB, may actually be initiated by the surgical procedure per se. Brasil and associates [13] reported a significantly higher release of tumor necrosis factor alpha in the CPB group when compared with off-pump surgery. Recent data from Tarnok and associates [20] suggest that similar increased serum levels of inflammatory mediators and increased consumption of complement and adhesion molecules occur during cardiovascular surgery either with or without CPB in children. They concluded that these changes are the combined effect of anesthesia, surgical trauma, and endothelial lesions.

Although the above studies [12, 13, 20] are appropriate in terms of control groups, none have been prospectively randomized. Other studies have added to the confusion by comparing cardiac operations carried out with CPB through median sternotomy with either noncardiac procedures such as abdominal aortic aneurysmectomy [21] or off-pump CABG performed through a minimally invasive approach [22].

To our knowledge, this is the first prospective randomized study reporting inflammatory responses of two similar cohorts of patients undergoing CABG with or without CPB. The attention placed in terms of patient selection and exclusion of factors potentially hiding the CPB-mediated IR should better clarify the specific role of the CPB itself.

Complement activation during CPB leads to the formation of the anaphylatoxins C3a and C5a mainly via the alternative pathway [1]. C3a usually peaks at the end of CPB [1], and this is known to be related to the duration of CPB [3]. Levels then return to pre-CPB values 24 to 48 hours postoperatively [1]. In accordance with other reports [1, 3], our study also showed a peak of complement activation soon after CPB. The mild elevation of C3a observed in the off-pump group could be related to the surgical manipulations, as suggested by Hahn-Pederson and associates [23]. C3a and C5a were significantly elevated at the end of surgery in the on-pump group when compared with both baseline value and the off-pump group. These results were obtained despite the lowering effect of hemodilution of the CPB prime, which is known to lower the concentrations of the inflammatory mediators [24]. However, comparison of data over time did not show any significant difference between the two groups.

The complement activation per se may lead to neutrophil activation [25]. Although the degree of inflammation induced by the activation of neutrophils is also thought to be related to the serum levels of IL-8, a major neutrophil chemotactic factor [26], and neutrophil elastase, a specific enzyme of neutrophils [25]. In keeping with these reports [26, 27], our study showed significantly higher levels of IL-8 and elastase soon after the end of CPB, with elastase remaining statistically higher during the entire observation period. WBC, neutrophil, and monocyte counts increased in both groups postoperatively, but more significantly in the CPB group. These data seem, therefore, to confirm the role of CPB as a main determinant of IR. The partial activation of similar mediators observed in the off-pump group suggests, however, that other facts like surgical maneuvers may to a less extent contribute to the IR.

However, the evaluation of postoperative morbidity is of the most value. Pulmonary dysfunction after CPB has been described in many studies as part of a systemic IR [1, 3], and has been related to pulmonary leukosequestration of neutrophils during CPB, with release of elastase, which may lead to lung parenchymal and endothelial injury [1, 3]. Our study showed a significantly higher incidence of chest infection and longer intubation times in the CPB group. Furthermore, we also revealeda statistically higher overall incidence of infections (based on positive culture of the specimens) in the on-pump group, suggesting a direct relation with CPB-mediated IR.

Blood loss and transfusion requirement were significantly decreased in the beating heart when compared with conventional CABG. Although blood loss seems high in the on-pump group of our study, these losses are in keeping with other recently published data [28]. Cell savers, transexamic acid, or aprotinin were not used in this study. In addition, eight patients in the on-pump group and seven in the off-pump group were unstable in-hospital referrals, managed preoperatively with aspirin and low molecular weight heparin, which have been reported to increase perioperative blood loss [29].

In conclusion, this study shows that off-pump coronary revascularization provides lower activation of the inflammatory mediators and reduced morbidity when compared with conventional surgery with CPB and cardioplegic arrest.

	Acknowledgments

 
This work was supported by the British Heart Foundation and the Garfield Weston Trust.

	References

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				E. L. Hannan, C. Wu, C. R. Smith, R. S.D. Higgins, R. E. Carlson, A. T. Culliford, J. P. Gold, and R. H. Jones Off-Pump Versus On-Pump Coronary Artery Bypass Graft Surgery: Differences in Short-Term Outcomes and in Long-Term Mortality and Need for Subsequent Revascularization Circulation, September 4, 2007; 116(10): 1145 - 1152. [Abstract] [Full Text] [PDF]

				S. Guizilini, W. J. Gomes, S. M. Faresin, D. W. Bolzan, E. Buffolo, A. C. Carvalho, and A. A.V. De Paola Influence of Pleurotomy on Pulmonary Function After Off-Pump Coronary Artery Bypass Grafting Ann. Thorac. Surg., September 1, 2007; 84(3): 817 - 822. [Abstract] [Full Text] [PDF]

				D. G. Healy, A. E. Wood, A. O'Neill, J. F. McCarthy, J. M. Fitzpatrick, and R. W. Watson Can preoperative modelling of individual neutrophil adhesion responses predict renal morbidity? Eur. J. Cardiothorac. Surg., June 1, 2007; 31(6): 1088 - 1093. [Abstract] [Full Text] [PDF]

				M. Glauber, A. Farneti, S. Bevilacqua, and J. Karimov Pump-assisted beating heart surgery MMCTS, February 19, 2007; 2007(0219): 943. [Abstract] [Full Text] [PDF]

				R. Motallebzadeh, J. M. Bland, H. S. Markus, J. C. Kaski, and M. Jahangiri Neurocognitive Function and Cerebral Emboli: Randomized Study of On-Pump Versus Off-Pump Coronary Artery Bypass Surgery Ann. Thorac. Surg., February 1, 2007; 83(2): 475 - 482. [Abstract] [Full Text] [PDF]

				S. J. Allen, W. T. McBride, T. J. McMurray, A. S. Phillips, S. P. Penugonda, G. Campalani, I. S. Young, and M. A. Armstrong Cell Salvage Alters the Systemic Inflammatory Response After Off-Pump Coronary Artery Bypass Grafting Surgery Ann. Thorac. Surg., February 1, 2007; 83(2): 578 - 585. [Abstract] [Full Text] [PDF]

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				M. R. Hoda, H. El-Achkar, E. Schmitz, T. Scheffold, H. O. Vetter, and R. De Simone Systemic Stress Hormone Response in Patients Undergoing Open Heart Surgery With or Without Cardiopulmonary Bypass Ann. Thorac. Surg., December 1, 2006; 82(6): 2179 - 2186. [Abstract] [Full Text] [PDF]

				H. Kamiya, T. Kofidis, A. Haverich, and U. Klima Preliminary experience with the mini-extracorporeal circulation system (Medtronic resting heart system) Interactive CardioVascular and Thoracic Surgery, December 1, 2006; 5(6): 680 - 682. [Abstract] [Full Text] [PDF]

				A. Sedrakyan, A. W. Wu, A. Parashar, E. B. Bass, and T. Treasure Off-Pump Surgery Is Associated With Reduced Occurrence of Stroke and Other Morbidity as Compared With Traditional Coronary Artery Bypass Grafting: A Meta-Analysis of Systematically Reviewed Trials * Supplemental Appendix I Stroke, November 1, 2006; 37(11): 2759 - 2769. [Full Text] [PDF]

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				M. E. Falagas, E. S. Rosmarakis, K. Rellos, A. Michalopoulos, G. Samonis, and S. N. Prapas Microbiologically documented nosocomial infections after coronary artery bypass surgery without cardiopulmonary bypass. J. Thorac. Cardiovasc. Surg., September 1, 2006; 132(3): 481 - 490. [Abstract] [Full Text] [PDF]

				G. Niranjan, G. Asimakopoulos, A. Karagounis, G. Cockerill, M. Thompson, and V. Chandrasekaran Effects of cell saver autologous blood transfusion on blood loss and homologous blood transfusion requirements in patients undergoing cardiac surgery on- versus off-cardiopulmonary bypass: a randomised trial. Eur. J. Cardiothorac. Surg., August 1, 2006; 30(2): 271 - 277. [Abstract] [Full Text] [PDF]

				K. G. Shann, D. S. Likosky, J. M. Murkin, R. A. Baker, Y. R. Baribeau, G. R. DeFoe, T. A. Dickinson, T. J. Gardner, H. P. Grocott, G. T. O'Connor, et al. An evidence-based review of the practice of cardiopulmonary bypass in adults: A focus on neurologic injury, glycemic control, hemodilution, and the inflammatory response. J. Thorac. Cardiovasc. Surg., August 1, 2006; 132(2): 283 - 290.e3. [Full Text] [PDF]

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				P. S. Lingaas, P. K. Hol, R. Lundblad, K. A. Rein, L. Mathisen, H.-J. Smith, R. Andersen, E. Thaulow, T. I. Tonnesen, J. L. Svennevig, et al. Clinical and Radiologic Outcome of Off-Pump Coronary Surgery at 12 Months Follow-Up: A Prospective Randomized Trial Ann. Thorac. Surg., June 1, 2006; 81(6): 2089 - 2095. [Abstract] [Full Text] [PDF]

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				P. McKeown and A. E. Epstein Future Directions: American College of Chest Physicians Guidelines for the Prevention and Management of Postoperative Atrial Fibrillation After Cardiac Surgery Chest, August 1, 2005; 128(2_suppl): 61S - 64S. [Abstract] [Full Text] [PDF]

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				Y. Naito, M. Nakajima, H. Inoue, and K. Tsuchiya Successful CABG in a patient with paroxysmal nocturnal hemoglobinuria Eur. J. Cardiothorac. Surg., March 1, 2004; 25(3): 468 - 470. [Abstract] [Full Text] [PDF]

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				A. M. Calafiore, M. Di Mauro, C. Canosa, G. Di Giammarco, A. L. Iaco, and M. Contini Myocardial revascularization with and without cardiopulmonary bypass: advantages, disadvantages and similarities Eur. J. Cardiothorac. Surg., December 1, 2003; 24(6): 953 - 960. [Abstract] [Full Text] [PDF]

				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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				W. Y. Thong, A. G. Strickler, S. Li, E. E. Stewart, C. L. Collier, W. K. Vaughn, and N. A. Nussmeier Hyperthermia in the Forty-Eight Hours After Cardiopulmonary Bypass Anesth. Analg., December 1, 2002; 95(6): 1489 - 1495. [Abstract] [Full Text] [PDF]

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