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Ann Thorac Surg 2008;85:543-547. doi:10.1016/j.athoracsur.2007.08.047
© 2008 The Society of Thoracic Surgeons
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Original Articles: Cardiovascular

Carbon Dioxide Field Flooding Reduces Neurologic Impairment After Open Heart Surgery

Sven Martens, MD, PhDa,*, Katrin Neumann, MD, PhDb, Christian Sodemann, MDa, Heinz Deschka, MDa, Gerhard Wimmer-Greinecker, MD, PhDa, Anton Moritz, MD, PhDa

a Department of Thoracic and Cardiovascular Surgery, Johann Wolfgang Goethe University, Frankfurt, Germany
b Department of Phoniatrics and Pediatric Audiology, Johann Wolfgang Goethe University, Frankfurt, Germany

Accepted for publication August 22, 2007.

* Address correspondence to Dr Martens, Department for Thoracic and Cardiovascular Surgery, Johann Wolfgang Goethe University-Hospital, Theodor Stern Kai 7, Frankfurt, 60590, Germany (Email: martens.herz{at}gmx.de).


   Abstract
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 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Air emboli released from incompletely deaired cardiac chambers may cause neurocognitive decline after open heart surgery. Carbon dioxide (CO2) field flooding is reported to reduce residual intracavital air during cardiac surgery. A protective effect of carbon dioxide insufflation on postoperative brain function remains unproven in clinical trials.

Methods: Eighty patients undergoing heart valve operations by median sternotomy were randomly assigned to either CO2 insufflation (group I, n = 39) or unprotected controls (group II, n = 41). Preoperative evaluation included neurocognitive test batteries consisting of six different tests, and objective measurements of brain function by means of P300 wave auditory-evoked potentials (peak latencies, ms). Neurocognitive testing and P300 measurements were repeated on postoperative day 5. Neurocognitive deficit (ND) was defined as a 20% decrement in two or more tests.

Results: Preoperatively, P300 peak latencies did not differ between groups (374 ± 75 vs 366 ± 72 ms, not significant [n.s.]). Five days after surgery, P300 peak latencies were significantly shorter with CO2 protection as compared with the unprotected control group (group I: 390 ± 68 ms, group II: 429 ± 75 ms, p = 0.02). Clinical outcome was comparable as for mortality (group I: 1 patient; group II: 2 patients) and cerebrovascular events or confusional syndromes (group I: 5 patients; group II: 4 patients) or other clinical variables as intubation time or hospital stay. Neurocognitive test batteries did not reveal differences between groups.

Conclusions: Shorter P300 peak latencies after surgery indicate less brain damage in patients who underwent heart valve operations with CO2 flooding of the thoracic cavity. Even if these findings were not supported by clinical results or neurocognitive test batteries in our cohort, carbon dioxide field flooding has proven efficiency and should be advocated for all patients undergoing open heart surgery.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Insufflation of carbon dioxide (CO2) into the operative field to prevent cerebral or myocardial damage by air embolism is reported since 1967 in open heart surgery [1]. Residual intracavital air, incompletely eliminated through standardized deairing procedures, is reported to result in central or peripheral organ gas embolization. In addition, gaseous microbubbles entering the cardiopulmonary bypass circuit lead to cerebral microembolization, contributing to postoperative cognitive impairment [2]. Despite carefully performed deairing procedures as puncturing of the left ventricle and the ascending aorta, transcranial Doppler studies revealed large amounts of emboli during the first ejections of the beating heart [3]. With the advent of minimally invasive valve surgery, deairing of the cardiac chambers has become more difficult and replacing air in the operative field by a more soluble gas has become a widely used technique in cardiac surgery. Manual deairing techniques have shown ineffectiveness in recent studies, and reduction of intracardiac bubbles through CO2 insufflation was demonstrated using echocardiography [4].

Carbon dioxide fills the thoracic cavity by gravity and replaces air if adequately insufflated. 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. In our institution, all patients undergoing open heart surgery are operated on with CO2 insufflation imperatively. The insufflation methods were optimized using a perforated drain sutured to the pericardium [6]. Our group has demonstrated the mild and transient effects of central CO2 embolism in contrast to air embolism in a porcine model using diffusion-weighted magnetic resonance imaging (MRI) [7]. However, a protective effect of carbon dioxide insufflation during open heart surgery on postoperative brain function remained unproven in clinical trials.

The P300 wave auditory-evoked potentials were suggested as an objective parameter for brain function [8]. Engelhardt and colleagues [9] and Grimm and colleagues [10] have shown applicability in cardiosurgical patient cohorts, and suggested P300 auditory-evoked potentials to be more sensitive for detection of minor neurocognitive deficits as compared to the widely used test batteries.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Eighty elective patients referred for open heart surgery by complete median sternotomy were randomized to either CO2 insufflation (group I, n = 39) or unprotected controls (group II, n = 41). All patients underwent Doppler screening of the extracranial cerebral vessels. Patients presenting with high grade stenoses of the carotid arteries (>70%) were excluded from the trial. The groups did not differ as to important cardiovascular risk factors (Table 1).


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  		Table 1 Preoperative Data
 
Carbon dioxide was applied from the start of the extracorporeal circuit using a perforated drain (Jackson-Pratt; Allegiance, McGraw Park, IL) in group I. Flow was directed into the surgical wound in order to flood the field by gravitation; gas flow was 2 L/minute, allowing for a CO2 content of greater than 90% in the thoracic cavity [6]. The surgical procedures specified in Table 2 were carried out after clamping and cross-sectioning of the ascending aorta or the left atrium, respectively. For both groups, deairing of the cardiac chambers was performed by the apex of the left ventricle in the Trendelenburg position. The aortic cross-clamp was then removed under continuous venting of the ascending aorta (and the left atrium in mitral valve procedures). Venting of the ascending aorta to evacuate residual gas was continued until the heart ejected and extracorporeal circuit was reduced.


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  		Table 2 Procedures and Perioperative Data
 
Neurocognitive outcome variables were selected according to the 1995 statement of consensus on assessment of neurobehavioral outcome after cardiac surgery [11]. Tests were performed preoperatively and 5 days after surgery. Results are reported as individual changes according to the guidelines of Stump [12] and group means. A decline in performance from the initial test interval that exceeded 20% in two tests or more was considered a deficit (ND). Our test battery included the Block design test (problem solving strategies, recognition, and analysis of forms), the Benton test (constructive abilities), the Trail making test (cognitive achievement at speed), the Digit span test (short term memory, memory of figures), and the d2 test (concentration performance). Testing was carried out by the same researcher (a trained member of our department) preoperatively and five days after surgery.

The P300 auditory-evoked potentials are the result of an activation of a widespread network of cortical structures as well as the hippocampus [13]. P300 is the term for a large positive-going peak in an averaged electroencephalogram (EEG) waveform, usually encountered after 300 ms. The P300 wave is characterized by the amplitude (mA) and latency (msec). It can be identified as the largest positive-going peak of the EEG waveform occurring after the earlier, exogenous components (N100, P200, N200) within a given latency window. As a result of the involvement of many brain regions, P300 can be used as a general indicator for neurocognitive function. The P300 latency reflects the speed of stimulus classification; it is negatively correlated with neurocognitive performance [14].

The P300 event-related potentials were recorded with silver/silver chloride electrodes on a Bio-logic Navigator PRO (Bio-logic Systems Corp, Mundelein, IL). The potentials were generated with a binaurally presented tone discrimination paradigm (odd-ball paradigm, 80% frequent tones of 1,000 Hz and 20% rare target tones of 2,000 Hz). The filter bandpass was set to 0.1 to 100 Hz and the tones were delivered at 55 dB hearing level. Active electrodes were placed at Cz (vertex) and Fz (frontal) positions and referenced to an earlobe A1/2 electrode (10/20 international system). The patients were instructed to keep their eyes closed and take a running mental count of the rare 2,000-Hz beep target tones. The P300 recordings with a discrepancy of greater than 10% between the actual number of stimuli and the number counted by the patients were rejected and repeated. At least two sets of measures were recorded in all patients before and after surgery. The recordings resulted in an order of positive and negative peaks. The latencies in milliseconds of the P300 peak were assessed. All measurements were performed by a physician in a noise-insulated room. All patients studied were free from narcotics or sedatives for at least 48 hours. The study was approved by our local ethics committee, and written informed consent was obtained from all patients.

Statistical analyses were carried out using the SPSS software package (SPSS Inc, Chicago, IL). In the absence of normal distribution, the Mann-Whitney U test was applied to compare differences between groups, while linear changes underwent the Wilcoxon signed rank test. Categoric variables were compared using the {chi}2 or Fishers exact tests as appropriate. Data are presented as mean ± standard deviation of mean. A p value below 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Mean operative time, extracorporeal circuit, and cross-clamp time were comparable (see Table 2). Preoperatively, P300 peak latencies did not differ between groups (374 ± 75 vs 366 ± 72 ms, not significant [n.s.]). Five days after surgery, P300 peak latencies were significantly prolonged without CO2 as compared with the protected group (group I: 390 ± 68 ms; group II: 429 ± 75ms, p = 0.02) (Fig 1). Clinical outcome was comparable for mortality and cerebrovascular events or confusional syndromes and other clinical variables as intubation time or hospital stay (see Table 3). In all seven patients with diagnosis of postoperative confusional syndrome, the status resolved within one to four days. Because of reduced physical or mental status after surgery and perioperative mortality, retesting with P300 auditory-evoked potentials could not be performed in four patients of group I and three patients of group II. Laboratory parameters of myocardial or renal damage did not differ between groups (Table 4).


Figure 1
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  		Fig 1. P300 peak latencies, before (left) and five days after surgery (right). Median, 25th/75th percentile and range are depicted. (Group I [CO2]; group II [control]; Cz = vertex; pre = preoperative; post = postoperative.)

 

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  		Table 3 Clinical Outcome
 

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  		Table 4 Laboratory Parameters
 
A neurocognitive deficit was revealed in 21 of 36 patients of group I (58%) and 24 of 38 patients of group II (63%, n.s.). See Table 5 for detailed results of group mean performances. Neurocognitive retesting after surgery could not be performed in three patients of each group for reduced physical or mental status, respectively.


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  		Table 5 Neurocognitive Tests
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
The clinical importance of gaseous microbubbles was largely underestimated in the past. However, the study of Borger and colleagues [2] successfully correlated cognitive outcome of cardiac patients to the number of interventions on extracorporeal circuit. Abu-Omar and colleagues [15] discriminated solid and gaseous microemboli during off-pump coronary artery bypass and on-pump coronary artery bypass (ONCAB) procedures, only 15% (ONCAB: 25%) were solid. They found a correlation between the number of microemboli and reduction of prefrontal activation using functional MRI. These findings underline the importance of a significant reduction of gas embolism in cardiac surgery.

Insufflation of CO2 is widely used in heart valve surgery, especially when minimally invasive approaches reduce the effectiveness of deairing procedures. In open heart surgery, the reduction of residual intracardiac bubbles with CO2 insufflation was demonstrated using echocardiography [4]. Air embolism has a deleterious effect on central organs, as demonstrated in a porcine model in 2004 by our group [7]. Cerebral embolization of the more soluble CO2 only leads to minor, mostly reversible lesions in diffusion-weighted MRI. Despite these marked differences, a protective effect of CO2 insufflation on postoperative cognitive performance remained unproven in clinical trials, probably because the insufflation methods were insufficient [16]. In addition, sensitivity of neurocognitive test scores, applied in the early postoperative period after cardiac surgery, for minor intergroup differences remains questionable. However, an important step toward improved organ protection was the validation of different insufflation methods and gas flows [6, 17].

In cardiosurgical patients, P300 was introduced as a diagnostic tool in 1995 [9]. No differences between preoperative and postoperative testing were found for the amplitude of the P300 wave, but for latency. The amplitude reflects the number of neurons involved in the task completion. A shorter latency of the P300 wave indicates better neurocognitive performance, because the neurons take a shorter time to process the signal. These results were enforced by the studies of Zimpfer and colleagues in 2003 [18]; P300 auditory-evoked potentials were significantly impaired compared with preoperative levels. Interestingly, in their study group (as in ours), standard psychometric tests failed to detect this subclinical cognitive impairment. Functional MRI detected significant relative reduction of prefrontal activation after ONCAB surgery, correlated with increased embolic load, but performance in verbal memory tasks was not impaired [15]. This emphasizes possible limitations of neurobehavioral test scores early after cardiac surgery.

Our objective measurements of P300 peak latencies revealed significantly better postoperative performance of CO2 protected patients. It is important to notice that all patients were operated on by complete median sternotomy. The deairing procedure included venting and deairing through the apex of the left ventricle, which is not possible in minimally invasive valve interventions (if partial sternotomy or right anterior thoracotomy is performed). In light of the presented data, we advocate CO2 insufflation not only for minimal invasive heart surgery, but for all cases in which (left sided) cardiac chambers are incised.

A limitation of the study was that we did not perform a late postoperative reevaluation of the patients with P300 auditory-evoked potentials. Zimpfer and colleagues [18] found that reversibility of impairment of peak latencies is dependent on patients age. Younger patients showed normalization of the initially impaired P300 peak latencies four months after aortic valve replacement, whereas the peak latencies of elderly patients remained prolonged. We think that the advantage of CO2 insufflation, a "cheap and easy" to perform protection method in open heart surgery, is proven with better neurocognitive performance early after surgery.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Selman MW, McAlpine WA, 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]
  2. Borger MA, Peniston CM, Weisel RD, Vasiliou M, Green REA, Feindl CM. Neuropsychologic impairment after coronary bypass surgery: effect of gaseous microemboli during perfusionist interventions J Thorac Cardiovasc Surg 2001;121:743-749.[Abstract/Free Full Text]
  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/Free Full Text]
  4. Svenarud P, Persson M, van der Linden J. Effect of CO2 insufflation on the number and behavior of air microemboli in open-heart surgery: a randomized clinical trial Circulation 2004;109:1127-1132.[Abstract/Free Full Text]
  5. Moore RM, Braselton CW. Injections of air and carbon dioxide into a pulmonary vein Ann Surg 1940;112:212-218.[Medline]
  6. Martens S, Dietrich M, Doss M, Wimmer-Greinecker G, Moritz A. Optimal carbon dioxide application for organ protection in open heart surgery J Thorac Cardiovasc Surg 2002;124:387-391.[Abstract/Free Full Text]
  7. Martens S, Theisen A, Balzer JO, et al. Improved cerebral protection through replacement of residual intracavital air by carbon dioxide: a porcine model using diffusion-weighted MRI J Thorac Cardiovasc Surg 2004;127:51-56.[Abstract/Free Full Text]
  8. Picton TW. The P300 wave of the human event related potential J Clin Neurophysiol 1992;9:456-497.[Medline]
  9. Engelhardt W, Dierks T, Pause M, Sold M, Hartung E, Silber R. P300-mapping—a neurophysiological tool to quantify cerebral dysfunction after coronary artery bypass grafting Eur J Cardiothorac Surg 1995;9:12-17.[Abstract/Free Full Text]
  10. Grimm M, Yeganehfar W, Laufer G, et al. Cyclosporine may affect improvement of brain function after successful cardiac transplantation Circulation 1996;94:1339-1345.[Abstract/Free Full Text]
  11. Murkin JM, Newman SP, Stump DA, Blumenthal JA. Statement of consensus on assessment of neurobehavioral outcomes after cardiac surgery Ann Thorac Surg 1995;59:1289-1295.[Free Full Text]
  12. Stump DA. Selection and clinical significance of neuropsychologic tests Ann Thorac Surg 1995;59:1340-1344.[Abstract/Free Full Text]
  13. Kiehl KA, Laurens KR, Duty TL, Forster BB, Liddle PF. Neuronal sources involved in auditory target detection and novelty processing: an event related fMRI study Psychophysiology 2001;38:133-142.[Medline]
  14. Polich J. P300 clinical utility and control of variability J Clin Neurophysiol 1998;15:14-33.[Medline]
  15. Abu-Omar Y, Cader S, Wolf LG, Pigott D, Matthews PM, Taggart DP. Short-term changes in cerebral activity in on-pump and off-pump cardiac surgery defined by functional magnetic resonance imaging and their relationship to microembolization J Thorac Cardiovasc Surg 2006;132:1119-1125.[Abstract/Free Full Text]
  16. Martens S, Dietrich M, Wals S, Steffen S, Wimmer-Greinecker G, Moritz A. Conventional carbon dioxide application does not reduce cerebral or myocardial damage in open heart surgery Ann Thorac Surg 2001;72:1940-1944.[Abstract/Free Full Text]
  17. Svenarud P, Persson M, Van der Linden J. Efficiency of a gas diffuser and influence of suction in carbon dioxide deairing of a cardiothoracic wound cavity model J Thorac Cardiovasc Surg 2003;125:1043-1049.[Abstract/Free Full Text]
  18. Zimpfer D, Kilo J, Czerny M, Kasimi MT, et al. Neurocognitive deficit following aortic valve replacement with biological/mechanical prosthesis Eur J Cardiothorac Surg 2003;23:544-551.[Abstract/Free Full Text]



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