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Ann Thorac Surg 2001;72:1940-1944
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Conventional carbon dioxide application does not reduce cerebral or myocardial damage in open heart surgery

Sven Martens, MD*a, Markus Dietrich, MDa, Stefanie Walsa, Sonja Steffena, Gerhard Wimmer-Greinecker, MD, PhDa, Anton Moritz, MD, PhDa

a Department for Thoracic and Cardiovascular Surgery, University Hospital J. W. Goethe, Frankfurt am Main, Germany

Accepted for publication August 8, 2001.

* Address reprint requests to Dr Martens, Klinikum der J. W. Goethe-Universität, Klinik für Thorax-Herz und thorakale Gefäßchirurgie, Theodor Stern Kai 7, D-60590 Frankfurt am Main, Germany
e-mail: martens.herz{at}gmx.de


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Open heart surgery is associated with a significant risk of cerebral and myocardial dysfunction, which is attributed in part to air embolism from incompletely deaired cardiac chambers. To evaluate the impact of carbon dioxide (CO2) insufflation to the thoracic cavity, a prospective randomized study was designed.

Methods. A total of 62 elective patients were randomly assigned to CO2 insufflation (group I, n = 31) or control (group II, n = 31). According to the Parsonnet risk score, 16 patients in group I (52%) and 10 patients in group II (32%) were categorized as being at either high risk or extremely high risk.

Results. In group II, perioperative mortality was 16.1% (5 patients); in group I, 1 patient died (ns). Creatine kinase MB isoenzyme, as a marker of myocardial damage, was more elevated in group I after surgery (38.0 ± 4.1 vs 28.0 ± 2.1, p = 0.02). Neurocognitive test scores did not reveal significant postoperative differences between groups.

Conclusions. Although mortality was lower with CO2 insufflation, no benefit could be demonstrated for markers of cardiac ischemic damage or neurocognitive outcome in this high-risk population. As CO2 concentrations in the thoracic cavity did not necessarily reach anticipated levels, our method of application is in question.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
In recent studies neurocognitive impairment has been shown in up to 88% of patients after cardiopulmonary bypass procedures; disturbances may be progressive and persistent [1]. Insufflation of carbon dioxide (CO2) to the operative field to prevent myocardial or cerebral damage by air embolism has been reported since 1957 in open heart surgery [2]. With the advent of minimally invasive valve surgery, deairing of the cardiac chambers has become more difficult, and replacement of air by a more soluble gas has become even more important. Despite careful deairing procedures, transcranial Doppler studies revealed a large amount of emboli during the first ejections of the beating heart [3]. Air emboli always remain in the arterial circulation until complete absorption; they only occasionally dislodge and flow downstream [4]. Because solubility of CO2 is better than that of air, occlusion or flow disruption in arteries of the brain or the heart is thought to be diminished. In 1940, Moore and Braselton [5] showed that the lethal dose of air was 12 times lower than that of CO2 injected into the pulmonary vein. Clinical benefit of CO2 insufflation to replace air in the thoracic cavity has not yet been proved in open heart surgery.

The aim of our study was to evaluate the clinical and biochemical benefit of a standardized, widely used method of CO2 application to the operative field in patients undergoing operation through a median sternotomy. Because most of the routine valve patients in our institution undergo operation through limited incisions, our study group mostly consists of combined procedures, representing a high-risk group of cardiac patients. In all of our patients who undergo valvular surgery through limited incisions, CO2 insufflation is standard.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
A total of 62 patients who underwent operation through a median sternotomy with opening of cardiac chambers were randomly assigned as follows: group I (n = 31 patients) received CO2 application, and group II (n = 31 patients) did not. Patients with a history of neurologic events or carotid stenosis were excluded from the trial. We used cardiotomy suction and venting through the apex of the left ventricle or the left atrium. The operations performed are summarized in Table 1; preoperative patients’ profiles and intraoperative data are shown in Table 2. Patients were categorized using the Parsonnet risk score [6]. In all, 16 patients in group I (52%) and 10 patients’ in group II (32%) were categorized as being at high risk or extremely high risk.


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  		Table 1. Operations Performed

 

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  		Table 2. Patient Characteristics

 
After anticoagulation by systemic administration of heparin (300 IU/kg Liquemin [Roche, Grenzach-Wyhlen, Germany]), cannulation of the ascending aorta was performed using a standard cannula (Jostra AG, Hirrlingen, Germany). For cannulation of the right atrium, we used a two-stage cannula or bicaval cannulation for mitral valve procedures, respectively (Jostra AG). Cardiopulmonary bypass was instituted with a Quadrox (Jostra AG) capillary membrane oxygenator. The circuit was primed with 1,500 mL of Ringer’s lactate solution, 500 mL of 6% hydroxyethyl starch, and 100 mL of 20% mannitol, and 150 IU/kg of heparin. Cardiopulmonary bypass was conducted with a flow of 2.4 L · min-1 · m-2 body surface area, rectal temperature was lowered to 30° ± 2°C, and alpha stat management was applied. Antegrade and retrograde cold blood cardioplegia were administered in an intermittent fashion, with reinfusions performed every 20 minutes. The arresting dose was 1,000 mL and the maintenance dose 400 mL. Anesthesia was maintained with sufentanyl, pancuronium, and propofol; ventilation was performed with a O2/N2O mixture establishing a FiO2 of 0.5 and aiming at a PCO2 of 35 to 40 mm Hg.

Carbon dioxide was applied using a perfusion line (2-mm inner diameter) sutured to the left sided pericardium. Flow was directed into the surgical wound to allow the gas to flood the field by gravitation; gas flow was 2000 cm3/min. Deairing of cardiac chambers was performed before release of the aortic cross-clamp through the apex of the left ventricle, the ascending aorta and the left atrium in mitral valve procedures. Venting through the ascending aorta was continued until the heart ejected blood and extracorporeal circuit was reduced.

Neurocognitive outcome variables were selected according to the 1995 Statement of Consensus on Assessment of Neurobehavioral Outcome after Cardiac Surgery [7]. Neurocognitive testing was carried out by the same researcher (a trained member of our department) preoperatively and 5 days after surgery. Results are presented as group means and according to the statement of consensus of 1997 [8], with analysis of individual changes following the guidelines of Stump [9]. A decline in performance from the initial test interval that exceeded 20% in two or more tests was considered to represent a deficit. Our test battery included Block design test (problem solving strategies, recognition and analysis of forms), Benton test (describing constructive abilities), Trail making (cognitive achievement at speed), Digit span (short-term memory, memory of figures) and d2 test (concentration performance).

Markers of cerebral (S100B, neuron specific enolase [NSE]) and myocardial (creatine kinase–MB, troponin-T) damage were taken preoperatively, 1 hour and 24 hours after surgery. S-100B and NSE served to quantify cerebral injury biochemically. S100B protein is a specific astroglial derivative. The S100B concentration was determined using a sensitive luminometric assay (Sanctec 100, Sangtec, Dietzenbach, Germany) that selectively measures the ß-subunits present in glial and Swann cells, according to the instructions of the manufacturer. The NSE serum concentration was measured using an enzyme-linked immunosorbent assay (Enzymun-Test NSE, Boehringer Mannheim Immunodiagnostica, Mannheim, Germany), with a detection limit of 0.5 µg/L. Serum concentration of troponin-T was also determined using an enzyme-linked immunosorbent assay (Enzymun-Test Troponin-T, Boehringer Mannheim).

The CO2 concentration in the operative field was measured in 10 additional patients (valve surgery and combined procedures with coronary artery bypass grafting respectively, cardiopulmonary bypass and CO2 application were conducted as described above) to verify our method of gas application. We used an infrared CO2 analyzer (BUSE, Bad Hönningen, Germany) which allowed continuous measurements with a sensitivity of 0.5%. The study was approved by our local ethics committee, and informed consent was obtained from all patients.

Statistical analysis was performed using the SAS software package (SAS, Cary, NC). The Mann-Whitney U test was used to compare differences between groups in the absence of normal distribution. Data are presented as mean ± standard error of mean. Fisher’s exact test was applied to test for significance in the difference in mortality and neurocognitive decline between groups. Differences were considered significant if the p value was less than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Mortality was 3% in group I (1 patient died of pulmonary failure 18 days after aortic valve replacement) versus 16.1% (5 patients) in group II (ns). All 5 patients died of low cardiac output or multiple organ failure between postoperative days 1 and 16. The operations performed were redo aortic valve replacement (1 patient), aortic valve replacement with coronary artery bypass grafting (2 patients), and mitral valve repair with coronary artery bypass grafting in 2 patients. In group I, patients were extubated 21.3 ± 3.1 hours after surgery; in group II extubation was performed 22.9 ± 3.4 hours after surgery (ns). Troponin T as marker of myocardial damage did not reveal significant differences between groups (Fig 1). Creatine kinase–MB was more elevated in the treatment group postoperatively and 24 hours after surgery (38.0 ± 4.1 vs 28.0 ± 2.1, p = 0.02, and 33.0 ± 3.8 vs 20.5 ± 2.4, p = 0.01, respectively). None of the tests performed revealed a significant impairment of neurocognitive function postoperatively (Table 3) if group mean scores are analyzed. The individual scores of 5 patients in group I (16%) declined more than 20% compared with their preoperative results in at least two tests on postoperative day 5. In group II, a decline was observed in 9 patients (29%). There were no statistically significant differences between groups. In group I, 2 patients exhibited prolonged confusion. In group II, 1 patient had a prolonged reversible ischemic neurologic deficit with hemiparesis on postoperative day 2. S100B was slightly lower with CO2 insufflation 1 hour after surgery (0.82 ± 0.46 vs 1.01 ± 0.99, ns), as shown in Figure 2. NSE was not different between groups (Fig 3).



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  		Fig 1. Changes in troponin T as a marker of myocardial damage. Time points: 1 = preoperatively; 2 = 1 hour postoperatively; 3 = 24 hours postoperatively. (CO2 = carbon dioxide.)

 

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  		Table 3. Neurocognitive Outcome

 


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  		Fig 2. Changes in S100B. Time points: 1 = preoperatively; 2 = 1 hour postoperatively; 3 = 24 hours postoperatively. (CO2 = carbon dioxide.)

 


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  		Fig 3. Changes in neuron specific enolase. Time points: 1 = preoperatively; 2 = 1 hour postoperatively; 3 = 24 hours postoperatively. (CO2 = carbon dioxide.)

 
To reveal the potential hazard of CO2 application, arterial blood samples were analyzed every 30 minutes while undergoing CPB. Results of partial pressure of CO2 are shown in Figure 4; PCO2 was significantly higher with gas insufflation 60 minutes after the start of CPB (p < 0.05). Measurements of CO2 concentration in the thoracic cavity showed levels between 8% and 86% (mean 44% ± 9%).



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  		Fig 4. Changes in arterial blood gas. (CO2 pre = PCO2 preoperatively; CO2 HLM = after start of cardiopulmonary bypass (CPB); CO2 30’, CO2 60’, CO2 90’, and CO2 120’ = after 30, 60, 90, and 120 minutes, respectively, of CPB; CO2 post = after CPB.) Differences are significant 60 minutes after the start of CPB (p < 0.05).

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Because insufflation of CO2 into the operative field is widely used in minimally invasive cardiac surgery, the aim of our study was to demonstrate a possible benefit for a group of high-risk patients who were undergoing operation through a median sternotomy. No benefit of carbon dioxide insufflation could be demonstrated in this group of patients. The difference in mortality and neurocognitive decline between groups was not statistically significant, but was remarkable for the fact that a higher percentage of patients in group I were considered to be at high risk or extremely high risk using the Parsonnet score. Biochemical markers of myocardial damage were less elevated in controls, with statistical significance for postoperative creatine kinase–MB, so slightly reduced mortality with CO2 insufflation could not be explained by reduction of myocardial damage in our study. Microembolization to other organ systems is a possible explanation for increased mortality in group II. Most valve operations are performed through limited incisions in our institution, which explains the higher risk profile of our study groups.

Neuropsychologic outcome and markers of cerebral damage were not significantly different between groups. The relevance of elevated serum levels of S100B is in question, because most serum S100B after CPB with cardiotomy suction is of extracerebral origin [10], but a significant increase has been reported in patients with cerebral damage compared with patients with uncomplicated outcomes after heart surgery [11, 12]. Regarding individual change scores, patients in our treatment group presented with fewer neurocognitive deficits, but the difference was without statistical significance. The study groups were definitely too small to reveal differences in mortality or in major neurologic adverse events. Neurocognitive test batteries are more sensitive for minor deficits, but the small size of our study groups limits the applicability of our findings.

There are several methods of CO2 application described in the literature. Many surgeons use standard perfusion lines with an inner diameter of 2 to 3 mm and a flow of 2 to 10 L/min CO2 to replace air in the thoracic cavity and cardiac chambers. Shang and colleagues [13] showed that a flow greater than 5 L/min was not more effective in replacing air from the thoracic cavity. Webb and colleagues [14] used a perforated commercial drain (Jackson Pratt; Allegiance Healthcare Corporation, Munich, Germany) and a flow of 10 L/min CO2; they showed a reduction in gas bubbles in the cardiac chambers visualized by transesophageal echocardiography. These investigators did not measure CO2 concentration in the operative field directly, but concluded from the concentration of oxygen that they reached CO2 concentrations of 93% or more. With our method of application, we reached mean CO2 levels of 44%, which suggests that it probably is less effective.

Several authors have described a rise in CO2 in the blood of patients with acidosis when CO2 was insufflated into the thoracic cavity [15–18]. This is dependent in part on the use of cardiotomy suction or venting. Methods have been described for monitoring CO2 levels in the cardiotomy reservoir and for preventing accumulation of CO2 with acidosis by flushing out excessive CO2 with oxygen [18]. To avoid critical systemic CO2 levels with acidosis, gas insufflation may be limited to the period immediately before release of the aortic cross-clamp. In our treatment group, CO2 partial pressure in arterial blood samples was significantly higher on bypass versus group II, but did not reach critical levels even when we used conventional cardiotomy suction and venting. For effective organ protection, elevated CO2 levels in cardiac chambers must be achieved before deairing and release of the aortic cross-clamp. Whether gas insufflation is mandatory during cross-clamping, with opening of cardiac chambers until deairing procedures are completed, or whether "washing out" residual air before release of the cross-clamp is sufficient, remains unknown.

Measurement of CO2 levels in the thoracic cavity showed low levels of CO2 with our method of application, which is used by many cardiac surgeons. With such low and variable levels of CO2, a protective function could not be proved in our study. For effective reduction of cerebral and coronary artery emboli, higher levels of CO2 must be achieved in the operative field by more sophisticated means of application.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. McKhann G.M., Goldsborough L.M., Borowicz M.S., et al. Cognitive outcome after coronary artery bypass: a one-year prospective study. Ann Thorac Surg 1997;63:510-515.[Abstract/Free Full Text]
  2. Selman M.W., McAlpine W.A., Albregt H., Ratan R. An effective method of replacing air in the chest with CO2 during open heart surgery. J Thorac Cardiovasc Surg 1967;53:618-622.[Medline]
  3. Van der Linden J., Casimir-Ahn H. When do cerebral emboli appear during open heart operations? A transcranial Doppler study. Ann Thorac Surg 1991;51:237-241.[Abstract]
  4. Branger A.B., Eckmann D.M. Theoretical and experimental intravascular gas embolism absorption dynamics. J Appl Physiol 1999;87:1287-1295.[Abstract/Free Full Text]
  5. Moore R.M., Braselton C.W. Injections of air and carbon dioxide into a pulmonary vein. Ann Surg 1940;112:212.[Medline]
  6. Parsonnet V., Dean D., Bernstein A.D. A method of uniform stratification of risk for evaluating the results of surgery in acquired adult heart disease. Circulation 1989;79(Suppl I):I3-I12.
  7. Murkin J.M., Newman S.P., Stump D.A., Blumenthal J.A. Statement of consensus on assessment of neurobehavioral outcomes after cardiac surgery. Ann Thorac Surg 1995;59:1289-1295.[Free Full Text]
  8. Murkin J.M., Stump D.A., Blumenthal J.A., McKhann G. Defining dysfunction: group means versus incidence analysis—a statement of consensus. Ann Thorac Surg 1997;64:904-905.
  9. Stump D.A. Selection and clinical significance of neuropsychologic tests. Ann Thorac Surg 1995;59:1340-1344.[Abstract/Free Full Text]
  10. Anderson R.E., Hansson L.O., Liska J., Settergren G., Vaage J. The effect of cardiotomy suction on the brain injury marker S100B after cardiopulmonary bypass. Ann Thorac Surg 2000;69:847-850.[Abstract/Free Full Text]
  11. Georgiadis D., Berger A., Kowatschev E., et al. Predictive value of S100B and neuron-specific enolase serum levels for adverse neurologic outcome after cardiac surgery. J Thorac Cardiovasc Surg 2000;119:138-147.[Abstract/Free Full Text]
  12. Wimmer-Greinecker G., Matheis G., Brieden M., et al. Neu-ropsychological changes after cardiopulmonary bypass grafting. Thorac Cardiovasc Surg 1998;46:207-212.[Medline]
  13. Shang W., Rosen M. Carbon dioxide in the prevention of air embolism during open heart surgery. Thorax 1968;23:194-196.[Abstract/Free Full Text]
  14. Webb W.R., Harrison L.H., Helmcke F.R., et al. Carbon dioxide field flooding minimizes residual intracardiac air after open heart operations. Ann Thorac Surg 1997;64:1489-1491.[Abstract/Free Full Text]
  15. Burbank A., Ferguson T.B., Burford T.H. Carbon dioxide flooding of the chest in open heart surgery. A potential hazard. J Thorac Cardiovasc Surg 1965;50:691-698.[Medline]
  16. Lippmann M. Complications of CO2 field flooding the surgical field in open heart surgery: an old technique revisited. Anesth Analg 1998;87:978.[Free Full Text]
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