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Ann Thorac Surg 2005;80:2326-2332
© 2005 The Society of Thoracic Surgeons

New technology

Miniaturized Cardiopulmonary Bypass in Coronary Artery Bypass Surgery: Marginal Impact on Inflammation and Coagulation but Loss of Safety Margins

Georg Nollert, MD a , * , Ina Schwabenland, MD a , Deniz Maktav, MD a , Felix Kur, MD a , Frank Christ, MD b , Peter Fraunberger, MD c , Bruno Reichart, MD a , Calin Vicol, MD a , 1

a Clinic of Cardiac Surgery, University of Munich, Munich, Germany
b Clinic of Anesthesiology, University of Munich, Munich, Germany
c Clinic of Clinical Chemistry, University of Munich, Munich, Germany

Accepted for publication May 17, 2005.

* Address correspondence to Dr Nollert, Clinic of Cardiac Surgery, University Clinic Munich, Clinic of Grosshadern, Marchioninistr 15, Munich 81366, Germany (Email: georg.nollert{at}med.uni-muenchen.de).


   Abstract
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PURPOSE: Inflammation and coagulation disturbances are common consequences of cardiopulmonary bypass (CPB). Recently, miniaturized closed CPB circuits without cardiotomy suction and venous reservoir have been proposed to reduce complication rates. We compared outcomes with conventional (CCPB) and miniaturized cardiopulmonary bypass (MCPB) after coronary artery bypass operations (CABG) with respect to inflammation and coagulation.

DESCRIPTION: Thirty patients (23% female; aged 67.9 ± 9.0 years) were prospectively randomly assigned to undergo isolated CABG with CCPB or MCPB. Conventional CPB had a pump prime of 1, 600 mL. Miniaturized CPB consisted of a centrifugal pump, arterial filter, heparinized tubing, and oxygenator with a priming volume of 800 mL. Shed blood was removed by a cell-saving device and reinfused. Measurements included interleukin (IL)-2 receptor, IL-6, IL-10, tumor necrosis factor receptor 55 and 75, C reactive protein, leukocyte differentiation, d-dimers, fibrinogen, and thrombocytes at six time points.

EVALUATION: In both groups no major complication occurred. However, two dangerous air leaks occurred in the closed MCPB circuit, demonstrating the narrow safety margins. Operative handling was also more difficult owing to limitations in venting and fluid management. International normalized ratio (p = 0.03) and antithrombin III (p = 0.04) levels were elevated during CPB in the CCPB group, most likely owing to differences of the intraoperative anticoagulation management. Repeated measures analysis revealed that not a single parameter of inflammation or clinical outcome showed significant differences among groups.

CONCLUSIONS: Use of a MCPB affected inflammation and coagulation variables only marginally and did not lead to clinical relevant changes as assessed by blood loss, need for blood products, and intensive care unit and clinical stays. However, safety margins for volume loss, air emboli, and weaning from CPB decrease, because of the closed MCPB circuit.


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Off-pump coronary artery bypass graft surgery (OPCABG) compared with on-pump surgery decreases the incidence of postoperative organ dysfunction particularly renal insufficiency and cerebral injury and the need for blood transfusions [1, 2]. A decreased inflammatory response with a minor production of proinflammatory cytokines is supposed to be one of the causes, and cardiopulmonary bypass is considered to be the culprit [3]. However, OPCABG may be technically challenging, cumbersome, and may have inferior surgical results with respect to long-term graft patency [4]. Therefore, miniaturized cardiopulmonary bypass (MCPB) systems have been developed to allow the ease of on-pump surgery (ie, an arrested heart) but avoiding or at least tempering the disadvantages [5]. Mayor differences to conventional cardiopulmonary bypass (CCPB) are use of heparinized tubing and oxygenators, minimizing prime volume, use of a centrifugal pump, and renunciation of cardiotomy suction and a venous reservoir. In a prospective randomized study, we compared the inflammatory response and clinical outcome among patients undergoing CABG with CCPB or MCPB. Our investigation was intended to investigate two completely different perfusion strategies, not just single components of the extracorporeal circuit.


   Material and Methods
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In 2003 and 2004, 30 consecutive patients undergoing elective, isolated CABG at our institution (77% male; mean age, 67.9 ± 9.0 years; range, 44 to 81; median, 70) gave informed consent for serving as subjects in this study. Institutional approval of the study was obtained from the Ethics Committee of the medical faculty, University of Munich (13.02.2003). The study was initially planned as a larger trial including 30 patients in each study arm. However, safety concerns (see Results) and no perceivable benefit for the patients in the MCPB group led to premature discontinuance of the study.

Patients with combined surgical procedures other than CABG were excluded from the study. Additional exclusion criteria were age younger than 18 years, weight greater than 80 kg, severe neurological or psychiatric disorder, acute infection, use of steroids, emergencies, myocardial infarction or use of clopidogrel within the preoperative week, coagulation disorders with international normalized ratio (INR) greater than 2, anemia with hemoglobin values less than 8 g/dL, terminal renal insufficiency with dialysis, oncologic diseases, reoperations, preoperative intraaortic balloon pump, and left ventricular ejection fraction less than 30%. Preoperative patient characteristics are summarized in Table 1.


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  		Table 1. Preoperative Patient Characteristics
 
Miniaturized CPB System
The heparin-coated closed tubing system (Carmeda coating; Medtronic, Minneapolis, Minnesoat) [6] included a heparin-coated oxygenator (Affinity NT Carmeda; Medtronic) and arterial filter (40 µ, Carmeda; Medtronic). The circuit without venous reservoir was customized for this study and driven by a centrifugal pump (BP 80, Medtronic). Priming (800 mL) included a balanced electrolyte solution (500 mL), hetastarch (100 mL), and 20% mannitol. A vent or a cardiotomy sucker was not part of the system; a cell-saving device was used for both purposes. Aprotinin was administered before (2 million IU) and during (0.5 million IU) CPB. Warm high potassium blood cardioplegia was initially applied (17 ± 2 mL) and intermittently repeated (23 ± 4 mL) according to Calafiore and colleagues [7]. Anticoagulation was achieved by heparin injection (150 IE/kg) and verified by an activated clotting time (ACT) of more than 250 seconds.

Conventional CPB System
A Sarns 9000 heart-lung machine with roller pumps, nonpulsatile flow mode, and membrane oxygenators (Affinity NT; Medtronic) was used for CPB. Tubing was not heparin coated and included cardiotomy suction, a venous reservoir (D744; Dideco, Mirandola, Italy), and filter in the arterial line (40 µ [Pall, East Hill, New York]). The priming volume of the circuit was 1,500 mL and consisted of a balanced electrolyte solution (500 mL), hetastarch (500 mL), sodium bicarbonate (8.4% 50 mL), additional aprotinin (200 mL; 2 million IU), and 20% mannitol (3 mL/kg body weight). Heparin (5,000 IE) was added to the prime. For systemic heparinization, 300 IE/kg was applied with a target ACT of more than 400 seconds. Cristalloid cardioplegia (Bretschneider HTK; Köhler Chemie, Germany), 1,142 ± 146 mL, was infused for cardiac arrest and repeated as needed (326 ± 204 mL).

General Anesthesia and Operative Management
Anesthesia was induced with etomidate 0.3 mg/kg, 0.3 µg/kg sufentanil, and 0.3 mg/kg midazolam. Each patient received 0.1 mg/kg pancuronium for muscle relaxation. After induction of anesthesia, controlled ventilation with a FiO2 of 0.5 was instituted. Anesthesia was maintained with fentanyl in increments of 0.5 mg as required and propofol in the MCPB group and with fentanyl and isoflurane 0.6% to 0.8% in the CCPB group. During CPB, a cardiac index of 2.4 L·min–1 ·m– 2, alpha-stat blood gas values and mild systemic hypothermia (esophageal temperature 32° ± 0.4°C) were used. After median sternotomy, the ascending aorta and the right atrial appendage were cannulated for arterial and venous access. In the MCPB group, the venous double-stage cannula was secured for air leaks by two pursestring sutures armed with Teflon pledgets (Impra, subsidiary of L.R. Bard, Tempe, Arizona) and, after an air leak occurred, two additional ligations around the atrial tissue were used. Operative data are summarized in Table 2.


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  		Table 2. Operative Data
 
Perioperative Measurements
Blood was withdrawn and analyzed in all patients at six different time points: (1) preoperatively, (2) 30 minutes after commencement of CPB, (3) 15 minutes after declamping the ascending aorta, (4) at the end of surgery, (5) 6 hours postoperatively, and (6) on the postoperative morning. Laboratory investigations included routine parameters (hemoglobin, creatine kinase, creatine kinase-MB, troponin I, blood cell count, and so forth) and measurements of interleukin (IL)-2 receptor, IL-6, IL-10, tumor necrosis factor receptor 55 and 75, C reactive protein, leukocyte differentiation, international normalized ratio, partial thromboplastin time, d-dimeres, fibrinogen, and thrombocytes at all time points. Because prime volume and hemodilution during CPB are different between the groups, all measurements are provided in Table 3 as original data and as data corrected for hemodilution. Original data are given, because the biological value of the parameters arguably depends on absolute values irrespective of hemodilution. For correction purposes, the preoperative hematocrit was chosen.


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  		Table 3. Perioperative Indications of Coagulation and Inflammation
 
Statistics
Values are expressed as mean and standard error of the mean. Differences among groups over time were tested for significant (p < 0.05) differences by two-way analysis of variance (ANOVA) with correction for repeated measures. Not time dependent differences among groups were tested with the Wilcoxon test. All statistical analyses were facilitated with the help of a statistical computer package (SPSS 12.0; SPSS, Chicago, Illinois).


   Results
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Clinical Outcome
All patients survived the operation and were discharged from the hospital (Table 4). One 61-year-old patient in the CCPB group had a large perioperative myocardial infarction (creatine kinase maximum 1,185 U/L, creatine kinase-MB 206 U/L, 167 ng/mL troponin I) due to an early saphenous vein graft occlusion to the right coronary artery. The surgeon considered the target vessel completely calcified and destroyed with insufficient run-off; the intraoperative bypass flow had been measured with 4 mL/min. A bypass revision was judged technically impossible in the hemodynamically stable patient. One patient in the MCPB group had postoperative agitated delirium, resulting in delayed wound healing and sternal instability. The patient had his sternum rewired on postoperative day 29. Miniaturized CPB had no significant impact on arterial blood pressure, use of inotropes, or ventilation (see Table 4). Intensive care unit stay (2.5 ± 0.4 versus 1.7 ± 0.3 days in the MCPB and CCPB groups, respectively; p = 0.35) and hospital stay (13.1 ± 2.5 versus 9.7 ± 0.9 days in the MCPB and CCPB groups, respectively; p = 0.23) did not differ significantly among groups.


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  		Table 4. Postoperative Outcome Measurements
 
Inflammation
Laboratory measurements of inflammation were not significantly different among groups neither for original nor for hematocrit-corrected values (Table 3). Only tumor necrosis factor-{alpha} receptor p55 levels tended (p = 0.08; see Fig 1) to be elevated during conventional CPB. However, the changes in tumor necrosis factor-{alpha} receptor p55 levels were much more pronounced in time than between groups.



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  		Fig 1. Laboratory indicators of inflammation and coagulation. Blood was withdrawn and analyzed in all patients at six different time points: (1) preoperatively, (2) 30 minutes after commencement of cardiopulmonary bypass, (3) 15 minutes after declamping the ascending aorta, (4) at the end of surgery, (5) 6 hours postoperatively, and (6) on the postoperative morning. The p values analyze differences among patients operated on with conventional cardiopulmonary bypass or a miniaturized cardiopulmonary bypass system over time (repeated measures analysis). As typical indicators of inflammation and coagulation, the results of fibrinogen (A) and tumor necrosis factor (TNF)–receptor 55 (B) are presented. All values are corrected for hemodilution. The course of the indicators measured is similar for both groups without evident differences. Data for all measurements are provided in Table 3.

 
Coagulation and Use of Blood Products
Coagulation tests show significantly higher levels of antithrombin and INR in the CCPB group (see Table 3). However, transfusion needs were similar. The MCPB patients received on average 0.4 ± 0.3 units fresh frozen plasma, 1.4 ± 0.4 units red blood cells, and 0.07 ± 0.07 units platelets compared with 0.3 ± 0.2 units fresh frozen plasma, 0.7 ± 0.3 units red blood cells, and 0 units platelets (p = 0.07 for fresh frozen plasma; p = 0.67 for red blood cells, and p = 0.07 for platelets).

Intraoperative Handling
In 2 patients, air entered the closed MCPB circuit. In the first case, the volume status of the patient was low and the negative pressure generated around the atrial cannula sucked small air bubbles into the venous cannula. Another ligation around the cannula resolved the problem, and the postoperative course was uneventful. In the second case, the left anterior descending artery running deep in the myocardium was dissected and the right ventricular cavity was opened unintentionally. Air was sucked into the MCPB, and the pump stopped immediately. After meticulous deairing and closure of the small right ventricular defect, the pump was started again. On the postoperative day, the patient was breathing spontaneously without any neuropsychological or neurologic deficit and had an otherwise uneventful course.

Volume management was more challenging in the MCPB group and consisted of intraoperative positioning of the patient (legs up and down) or application of a vasoconstrictor (norepinephrin). However, episodes of low venous return during surgery were not uncommon. Another issue in the MCPB group was the limited option of venting. Venting was performed through a needle vent in the ascending aorta discontinuously connected to a cell-saving device to limit blood loss. Therefore, a blood-filled left ventricle and coronary blood flow made surgery less comfortable.


   Comment
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 Material and Methods
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We discontinued the study prematurely because we were concerned with the safety of the MCPB system. Air had entered the closed system in 2 of 15 cases. In the first case, the air was sucked in the right atrium through a double pursestring suture armed with Teflon pledgets around the right atrial cannula in the atrial appendage. This air leak is certainly avoidable, and we changed the operative technique and used additional tight ligations around the cannula and the atrial tissue. After the change in technique, a similar air leak was never encountered again. However, the second case of air leak with an unintentional defect in the right ventricle caused by preparation of an intramyocardial LAD clearly demonstrates the low safety margins of the MCPB system.

The MCPB system has several at least theoretical advantages over the CCPB system. Renunciation of a cardiotomy sucker connected to a venous reservoir avoids direct reinfusion of air activated blood that may also be contaminated with tissue debris and lipids. It has been shown that cardiotomy suction and blood air contact in a venous reservoir may cause hemolysis, inflammation, lipid embolism, and coagulation disturbances [8–11]. Other advantageous techniques particularly reducing the prime volume [12], use of heparin-coated tubing and oxygenators [13, 14], as well as centrifugal instead of roller pumps [6], and warm blood cardioplegia according to Calafiore and associates [7] are not restricted to MCPB systems, but may be an integral part of any CPB system.

When we designed the study, we expected the upper limit of differences among CCPB and MCPB systems to be the previous published differences between OPCABG and on-pump surgery. However, we were not able to demonstrate any significant benefit for patients operated on with the MCPB system, although we used very sensitive laboratory parameters of inflammation and coagulation instead of clinical data as endpoints [14, 15]. Clinical outcome parameters such as use of blood products, perioperative complications, ventilation time, and intensive care unit stay were not expected to vary significantly among groups, because previous comparisons between OPCABG and on-pump surgery needed large patient populations to demonstrate meaningful differences [16]. In this study, however, we were unable to detect even a trend toward a better outcome in MCPB patients (see Table 3). Other studies reporting on MCPB systems confirm our results. Fromes and coworkers [17] report similar clinical outcomes with a trend toward longer pump runs (p = 0.05) in the MCPB group, which is consistent with our data and may explained by the more demanding technique. The authors describe a reduction in the inflammatory response although they report only a single difference in absolute values, namely, IL-6 (p = 0.04), is lower in the MCPB group at the end of CPB. This result is not corrected for multiple measurements. In a recent retrospective study [4] with approximately 1,000 patients, mortality rate, ventilation time, and intensive care unit and hospital stays were similar in the MCPB and CCPB groups, although postoperative complications and transfusion needs were lower in the MCPB group.

Limited venting possibilities, air leaks, and difficult volume management in the presence of massive bleeding make surgery using a MCPB system more cumbersome or even dangerous. New developments of MCPB systems realized these shortcomings. Air filters, vents, and even cardiotomy suckers have been added to recent systems to facilitate open heart surgery and valve replacements procedures. However, the original ideas of MCPB systems—avoidance of blood air contact, minimizing the prime volume, and cleaning shed blood before retransfusion to reduce blood activation and lipid embolism—are counteracted by these developments. The idea of MCPB systems has initiated important new efforts within science and industry to improve the biocompatibility of CPB systems. Clinical advantages for patient undergoing cardiac surgery need to be defined in future studies.


   Disclosures and Freedom of Investigation
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Medtronic, Inc, funded the laboratory investigations and documentation of the study. All cardiopulmonary bypass circuits, oxygenators, and further equipment were purchased. The authors had full control of the design of the study, methods used, outcome parameters, analysis of data, and production of the written report.


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Disclaimer The Society of Thoracic Surgeons, the Southern Thoracic Surgical Association, and The Annals of Thoracic Surgery neither endorse nor discourage use of the new technology described in this article.

1 Dr Vicol discloses a financial relationship with Medtronic, Inc. Back


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  1. Puskas JD, Thourani VH, Marshall JJ, et al. Clinical outcomes, angiographic patency, and resource utilization in 200 consecutive off-pump coronary bypass patients Ann Thorac Surg 2001;71:1477-1483.[Abstract/Free Full Text]
  2. Gummert JF, Bucerius J, Walther T, et al. Requirement for renal replacement therapy in patients undergoing cardiac surgery Thorac Cardiovasc Surg 2004;52:70-76.[Medline]
  3. Wan IY, Arifi AA, Wan S, et al. Beating heart revascularization with or without cardiopulmonary bypassevaluation of inflammatory response in a prospective randomized study. J Thorac Cardiovasc Surg 2004;127:1624-1631.[Abstract/Free Full Text]
  4. Khan NE, De Souza A, Mister R, et al. A randomized comparison of off-pump and on-pump multivessel coronary-artery bypass surgery N Engl J Med 2004;350:21-28.[Abstract/Free Full Text]
  5. Wiesenack C, Liebold A, Philipp A, et al. Four years' experience with a miniaturized extracorporeal circulation system and its influence on clinical outcome Artif Organs 2004;28:1082-1088.[Medline]
  6. Moen O, Fosse E, Dregelid E, et al. Centrifugal pump and heparin coating improves cardiopulmonary bypass biocompatibility Ann Thorac Surg 1996;62:1134-1140.[Abstract/Free Full Text]
  7. Caputo M, Bryan AJ, Calafiore AM, Suleiman MS, Angelini GD. Intermittent antegrade hyperkalaemic warm blood cardioplegia supplemented with magnesium prevents myocardial substrate derangement in patients undergoing coronary artery bypass surgery Eur J Cardiothorac Surg 1998;14:596-601.
  8. Jewell AE, Akowuah EF, Suvarna SK, Braidley P, Hopkinson D, Cooper G. A prospective randomised comparison of cardiotomy suction and cell saver for recycling shed blood during cardiac surgery Eur J Cardiothorac Surg 2003;23:633-636.[Abstract/Free Full Text]
  9. Svenmarker S, Engstrom KG. The inflammatory response to recycled pericardial suction blood and the influence of cell-saving Scand Cardiovasc J 2003;37:158-164.[Medline]
  10. Appelblad M, Engstrom G. Fat contamination of pericardial suction blood and its influence on in vitro capillary-pore flow properties in patients undergoing routine coronary artery bypass grafting J Thorac Cardiovasc Surg 2002;124:377-386.[Abstract/Free Full Text]
  11. Aldea GS, Soltow LO, Chandler WL, et al. Limitation of thrombin generation, platelet activation, and inflammation by elimination of cardiotomy suction in patients undergoing coronary artery bypass grafting treated with heparin-bonded circuits J Thorac Cardiovasc Surg 2002;123:742-755.[Abstract/Free Full Text]
  12. Shapira OM, Aldea GS, Treanor PR, et al. Reduction of allogeneic blood transfusions after open heart operations by lowering cardiopulmonary bypass prime volume Ann Thorac Surg 1998;65:724-730.[Abstract/Free Full Text]
  13. Ovrum E, Holen EA, Tangen G, et al. Completely heparinized cardiopulmonary bypass and reduced systemic heparinclinical and hemostatic effects. Ann Thorac Surg 1995;60:365-371.[Abstract/Free Full Text]
  14. Asimakopoulos G. Systemic inflammation and cardiac surgeryan update. Perfusion 2001;16:353-360.[Abstract/Free Full Text]
  15. Peschon JJ, Torrance DS, Stocking KL, et al. TNF receptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation J Immunol 1998;160:943-952.[Abstract/Free Full Text]
  16. Puskas JD, Williams WH, Mahoney EM, et al. Off-pump vs conventional coronary artery bypass grafting: early and 1-year graft patency, cost, and quality-of-life outcomes. A randomized trial JAMA 2004;291:1841-1849.[Abstract/Free Full Text]
  17. Fromes Y, Gaillard D, Ponzio O, et al. Reduction of the inflammatory response following coronary bypass grafting with total minimal extracorporeal circulation Eur J Cardiothorac Surg 2002;22:527-533.[Abstract/Free Full Text]



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