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Ann Thorac Surg 2003;76:1516-1522
© 2003 The Society of Thoracic Surgeons
a Bristol Heart Institute, University of Bristol, Bristol, United Kingdom
Accepted for publication May 2, 2003.
* Address reprint requests to Dr Ascione, Cardiothoracic Surgery, Bristol Heart Institute, Bristol Royal Infirmary, Bristol BS2 8HW, United Kingdom
e-mail: r.ascione{at}bristol.ac.uk
Abstract
BACKGROUND: We investigated the changes occurring in cerebral cortical oxygenation during off-pump coronary artery bypass (OPCAB) surgery using near infrared spectroscopy (NIRS).
METHODS: Measurement of cerebral cortical oxygenation changes included concentration of deoxygenated hemoglobin [HHb], oxygenated hemoglobin [O2Hb], changes in the redox status of the cytochrome c oxidase [Cyt-Ox], cerebral saturation as expressed by the tissue oxygenation index (TOI), and cerebral blood volume (CBV) as expressed by tissue hemoglobin index (THI). Measurements were performed in 23 consecutive patients during grafting of: left anterior descending (LAD setup 1; n = 23), posterior descending (PDA setup 2; n = 17), and Circumflex (Cx setup 3; n = 19) coronary arteries. Measurements were performed before any surgical manipulation (baseline), following positioning of the pressure stabilizer during construction of the distal anastomosis and 2 minutes after the completion of each distal anastomosis with the heart returned to its natural position.
RESULTS: There were no in-hospital deaths, neurologic deficits, or myocardial infarcts. Compared to baseline, during LAD grafting there was a marked reduction in [O2Hb] [-1.08 (-1.77 to -0.39), mean difference (95% CI) (p < 0.0008)], without a significant change in [HHb]. There was also a 4% reduction in cerebral saturation and a 3% fall in CBV (both p < 0.05). Setup 2 (PDA) was associated with a marked decrease of [O2Hb] [-1.92 (-2.95 to -0.88) mean difference (95% CI) (p < 0.0025)], which was accompanied by an increase in [HHb] [1.89 (1.00 to 2.77) mean difference (95% CI) (p < 0.0025)], and a 4% reduction in cerebral saturation (p < 0.0008). Grafting of the Cx was associated with a marked increase in [HHb] [2.85 (1.46 to 4.2) mean difference (95% CI) (p < 0.0025)], with no changes in [O2Hb], a 6% reduction in cerebral saturation, and a 12% increase in CBV (both p < 0.05). In all 3 settings, however, the changes were not associated with a modification in the redox state of [Cyt-Ox]. On returning to baseline condition, the changes in [O2Hb] and TOI observed in setup 1 persisted, and a significant reduction was observed in the redox state of the [Cyt-Ox] when compared with baseline [-0.08 (-0.14 to -0.02) mean difference (95% CI) (p < 0.002)]. For setups 2 and 3 there was recovery of the cerebral cortical oxygenation.
CONCLUSIONS: Grafting of the LAD on the beating heart is responsible for changes in cerebral cortical oxygenation which persist early after returning the heart to its natural position. Grafting of the Cx and PDA result in transient reversible changes. Trendelenburg positioning and right lateral tilting of the operating table during grafting of lateral and posterior walls might have a protective role in preventing cerebral cortical ischemia. Further studies are needed to assess the clinical importance of these observations.
Near infrared spectroscopy (NIRS) is a well-developed technique that allows noninvasive monitoring of regional changes in cortical tissue oxygenation in response to various stimuli [1–4]. It permits monitoring of several markers of cerebral cortical oxygenation including concentration of deoxygenated hemoglobin [HHb], oxygenated hemoglobin [O2Hb], changes in the redox status of the cytochrome c oxidase [Cyt-Ox], cerebral saturation as expressed by the tissue oxygenation index (TOI), and changes in tissue hemoglobin index (THI). In the absence of hemodilution, changes in THI should reflect changes in cerebral blood volume (CBV) [3, 4].
Cerebral injury still remains a major complication in patients undergoing coronary artery surgery [5, 6]. Off-pump coronary artery bypass (OPCAB) surgery has become more and more popular worldwide over the past decade [7, 8], in an attempt to minimize complications associated with cardiopulmonary bypass (CPB). There is, however, controversial evidence in the literature on the beneficial effect of OPCAB surgery on cerebral function [9–15]. During OPCAB surgery, heart manipulations are needed to facilitate exposure and grafting of each of the three main coronary territories. Exposure, positioning, and stabilization of each coronary target have been associated to temporary, clinically insignificant hemodynamic changes [16]. However, it remains uncertain to what extent these might affect cerebral cortical oxygenation.
The aim of the present study is to evaluate the changes in cerebral cortical oxygenation occurring during OPCAB surgery.
Patients and methods
Patient selection
Eligibility for surgery was based on the medical history and a recent coronary angiogram. Exclusion criteria included: history of head trauma or stroke causing significant active neurologic disease, a history of neurosurgery, severe or symptomatic carotid artery disease, left ventricular ejection fraction (EF) of less than 40%, recent myocardial infarction (MI) (< 1 month), reoperation, single vessel coronary disease. No exclusion criteria were applied with relation to the anatomic position and size of the coronary vessel to be grafted.
The study was approved by the United Bristol Healthcare Trust Ethics Committee and all patients gave informed consent.
Anesthetic technique
A standardized anesthetic technique was used for all patients. Patients were premedicated with a benzodiazepine and induction of anesthesia was carried out with Midazolam 0 to 4mg, Fentanyl 10 to 15 &mug/kg, Propofol 0 to 1.5 mg/kg, and neuromuscular blockade achieved with Pancuronium 0.15 mg/kg. Maintenance of anesthesia was carried out with Midazolam 0 to 0.2 mg/kg, Fentanyl 0 to 15 &mug/kg, and Propofol Infusion at 2 to 5 mg · kg-1 · h-1. The lungs were ventilated to achieve normocapnia with air and oxygen (FiO2=0.45 to 0.5). End tidal carbon dioxide was maintained between 35 and 40 mm Hg throughout. Invasive blood pressure, heart rate, and noninvasive arterial saturation were monitored using a Marquette patient monitoring system (Solar 8000 Patient Monitor, Marquette Medical Systems, Milwaukee, WI). Mean arterial pressure was maintained between 50 and 100 mm Hg with metaraminol or volume as appropriate. Heparin 150 IU/kg was administered before the start of the first anastomosis to achieve an activated clotting time (ACT) between 250 to 350 seconds. On completion of all anastomoses, protamine sulfate was given to reverse the effect of heparin and return the ACT to less than 140 seconds.
Surgical technique
The surgical technique and the settings for grafting of the three main coronary arteries have been previously described [9]. All patients underwent standard median sternotomy. Briefly, a half-folded swab (12 cm wide and 70 cm long) is snared to the posterior pericardium, halfway between the inferior vena cava and the left inferior pulmonary vein. Traction is applied on the two limbs of the swab and the snare. These are then fixed to the surgical drapes to facilitate exposure of the target coronary vessels which are then stabilized with a reusable stainless steel pressure stabilizer developed at our institution. All anastomoses are performed with an intracoronary shunt to ensure distal perfusion.
For setup 1 (left anterior descending=LAD) the operating table is kept in a flat position. For setups 2 and 3 (posterior descending=PDA and Circumflex=Cx, respectively) the operating table is positioned in Trendelenburg at about 20 degrees; and rotated 30 degrees towards the surgeon [10] to increase venous return and facilitate the spontaneous anticlockwise rotation of the beating heart to the right.
NIRS principles
Near infrared light in the wavelength range between 700 and 1000 nm penetrates biological tissue and bone quite well, which makes transcranial measurements through the intact skull and scalp feasible [17]. The technique of NIRS relies on the application of a modified Lambert-Beer law for the calculation of changes in the concentration of tissue chromophores from measured variations in attenuation of light, which depends on scattering and absorption of the investigated medium [17, 18]. Changes in concentration of a number of chromophores can be computed simultaneously from the changes in attenuation at a number of wavelengths using a least square regression algorithm incorporating the relevant extinction coefficients for each wavelength and chromophore [19].
Changes of cerebral cortical oxygenation measurable with NIRS include concentration of deoxygenated hemoglobin [HHb], oxygenated hemoglobin [O2Hb], changes in the redox status of the cytochrome c oxidase [Cyt-Ox], a putative parameter for cellular oxygenation [2], cerebral saturation as expressed by the tissue oxygenation index (TOI), which is the ratio of oxygenated to total tissue hemoglobin, and changes in the tissue hemoglobin index (THI). The latter represents the total amount of hemoglobin in the tissue under investigation. This has two components, the concentration of hemoglobin in blood and the volume of blood in the brain. In the absence of hemodilution, changes in THI should reflect changes in cerebral blood volume [3, 4]. Changes in CBV from baseline can be calculated using the equation 
CBV = HbT (0.89/Hb), where HbT is the sum of [O2Hb] and [HHb] and Hb is the blood hemoglobin concentration, which was measured serially according to the time points for NIRS monitoring.
NIRS monitoring
Monitoring commenced at chest incision and continued until the end of surgery. Head up, head down, and right tilt changes in table position made during the surgery were recorded with a leveling device. Measurements were performed before any surgical manipulation (baseline), after 2 minutes following positioning of the pressure stabilizer during construction of distal anastomoses and 2 minutes after the completion of each distal anastomosis, with the heart returned to its baseline position. At each time point, data were recorded at 0.5-second intervals and averaged into 30-second epochs. Changes in [O2Hb], [HHb], [Cyt-Ox], (TOI), and (THI) were recorded using a NIRO 300 near infrared spectroscope (Hamamatsu Photonics KK, Hamamatsu City, Japan). The NIR light transmitting optode and the light detector were located in the right frontal region just below the hairline avoiding the temporalis muscle and midline sinuses. An interoptode spacing of 5 cm was used and the optode and detectors were secured with a double sided adhesive dressing and a self-adherent wrap. The optodes were then shielded from ambient light. A pathlength factor of 6.0 was used to correct for the multiple light scattering effects of biological tissues [20]. A personal computer with NIRO 3000L software was connected to the system to download data.
Hemodynamic monitoring
Blood pressure (systolic, diastolic, and mean), heart rate, central venous pressure (CVP), and arterial saturation were monitored using a Marquette patient monitoring system (Solar 8000 Patient Monitor, Marquette Medical Systems, Milwaukee, WI). Parameters were recorded before any cardiac manipulation (baseline), in setups 1, 2, and 3, after the completion of each distal anastomosis with the patient and the heart returned to their baseline position.
Statistical analysis
Results are expressed as means ±SD for baseline values, and the difference of the mean with upper and lower 95% confidence intervals for the exposed stabilized and released positions for each variable. Paired t tests with Bonferonni's correction were used for analysis. A p value of less than 0.05 was considered a statistically significant difference. All analyses were performed using SAS release 8.1 (SAS Institute, Inc, Cary, NC).
Results
The clinical study involved 23 patients (19 male, mean age 60.7 ± 8.2 years). The mean number of grafts performed was 2.8 ± 1. In total there were 23 LAD grafts, 17 PDA, and 19 Cx. The mean duration of NIRS measurement was 217 ± 32 minutes. The mean duration for LAD grafting was 17 ± 5 minutes, for PDA 16 ± 4 minutes, and for Cx 22 ± 10 minutes. All patients completed the study. There was no in-hospital death, neurologic deficit, or myocardial infarction. Postoperative complications only included 4 (17.4%) atrial fibrillations and 2 (8.7%) chest infections. Mean postoperative hospital stay was 5.6 ± 0.9 days. At a mean followup of 25 months (range from 10 to 34 months) all patients remained symptom free, with no late neurologic complications.
Hemodynamic results
Hemodynamic
parameters are reported (Tables 1–3) for each respective setup.
These only showed a transient increase of central
venous pressure during setups 2 and 3 when compared to baseline (both p = 0.01). In both settings the CVP returned to baseline levels on returning the heart and the operating table to natural position.
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Setup 2: PDa
During setup 2 there was a marked decrease in [O2Hb] (p < 0.0025) that was accompanied by an increase in [HHb] (p < 0.0025). These changes were reflected in a 4% reduction in cerebral saturation (p < 0.0008) when compared to baseline values. No differences were observed in the redox state of cytochrome oxidase. Following return to baseline conditions there was a rapid reversal of these changes (Table 2).
Setup 3: Cx
During setup 3 there was an increase in [HHb] (p < 0.0025) that was not associated with changes in [O2Hb] and was accompanied by a 12% rise in CBV (p < 0.02) and a 6% reduction in cerebral saturation (p < 0.0002). The redox state of cytochrome oxidase was unaltered compared to baseline. Following release of positioning maneuvers all values returned to baseline (Table 3).
Comment
Neurologic complications now constitute a growing percentage of serious postoperative morbidity following coronary surgery, largely as a result of factors related to the increasing age of the surgical population [6, 21]. Hypoperfusion during CPB [22], microemboli of gaseous or particulate nature [23], or the result of inflammatory changes that lead to increase in permeability across the blood-brain barrier with resultant cerebral edema [24] have been identified as common causes. There are a number of difficulties in assessing and quantifying cerebral injury postcardiac surgery. Several studies have questioned the validity of S100 as a marker of neurologic injury, postulating that mechanisms other than the type of surgery used may determine or prevent the release of S100 including the absence or presence of line filters, the use of cardiotomy suction during the period of CPB, or postoperative autotransfusion [25]. Also, there are inherent difficulties associated with the detection of functional, subclinical problems such as cognitive dysfunction including memory and attention [26].
Over the last decade, NIRS technology has been used routinely by vascular surgeons during carotid endarterectomy to monitor cerebral cortical oxygenation [27]. Conversely, little is reported in the literature on the use of this monitoring technique during cardiac surgery in which the potential of cerebral dysfunction remains high.
In this study, NIRS technology has been used to ascertain the impact of OPCAB surgery on cerebral cortical oxygenation. To our surprise, grafting of the LAD was to cause the most evident changes in cerebral cortical oxygenation. These consisted in a marked decrease in [O2Hb], cerebral saturation, and CBV. Most importantly, on returning to baseline condition, the changes in [O2Hb] and cerebral saturation persisted, while a new change was observed in the redox state of the cytochrome oxidase when compared with baseline. Our technique of exposure and stabilization, when grafting the LAD, does not require either head-down tilting or rotation of the operating table. This might explain the marked reduction in CBV, which suggests that there was less blood in the scanned cerebral field. In turn, this might account for the derangement in the redox state of the cytochrome oxidase on returning to baseline conditions. Furthermore, the concomitant finding that the [HHb], which is almost nonexistent in the arterial compartment, did not change would also suggest a reduction in the size of the arterial compartment.
The observed changes during grafting of both the PDA and the circumflex territories involved, differently, the investigated markers of cerebral cortical oxygenation when compared with setup 1. Particularly, setup 2 showed a marked decrease in [O2Hb] that was accompanied by a marked increase in [HHb]. Simultaneously, there was a 4% reduction in cerebral saturation with no change in CBV. During setup 3 there was a marked increase in [HHb] that was not associated with changes in [O2Hb]. Concomitantly, there was a 12% rise in CBV, and a 6% reduction in cerebral saturation. The changes observed during setups 2 and 3 are more likely to be associated with Trendelenburg positioning and right lateral tilting of the operating table. These positioning maneuvers have been associated with an elevation of intracranial pressure and central venous pressure [28, 29]. This may determine a reduction of cerebral perfusion pressure, which in turn may affect cerebral blood flow and explain the increase in [HHb].
The findings of the present study might be due either to embolic phenomena or to cerebral hypoperfusion. However, ascending aorta manipulation, a recognized risk factor for cerebral embolization, was absent during LAD grafting due to the use of a pedicled mammary artery. It is, however, likely that temporary cerebral hypoperfusion due to patient and (or) heart positioning might have triggered the observed changes.
The clinical importance of these findings, however, needs to be further investigated as most of them recovered to baseline values after the release of the positioning maneuvers and were not associated with changes in the redox state of cytochrome oxidase, the most important indicator of cellular ischemia [2]. Surprisingly, the only change in the redox state of cytochrome oxidase was seen on returning to baseline condition after LAD grafting, which was the only setting determining a reduction of CBV. This might suggest that Trendelenburg positioning and right lateral tilting of the operating table, used at our institution only for Cx and PDA grafting, might prevent such changes.
Cooper and Springett showed that marked changes in the redox state of cytochrome oxidase only occur after prolonged highly significant changes in cerebral oxygenation [2], which was not the case for any setting of the present study.
Kirkpatrick and colleagues established [30] the threshold for severe cerebral ischemia (SCI) by using near infrared spectroscopy in the adult undergoing carotid endarterectomy. An intraoperative fall in transcranial Doppler-detected middle cerebral artery flow velocity of greater than 60%, accompanied by a sustained fall in cortical electrical activity, were adopted as criteria for SCI. Ipsilateral frontal NIRS recorded the total difference in [HHb] and [O2Hb]. Interrupted time series analysis following clamping of the internal carotid artery (ICA) allowed the different vascular components of ICA deltaHb to be identified. Within the resolution of the criteria used an ICA deltaHb threshold of 6.8 micromol/L provided 100% specificity for SCI. In our study, out of 23 patients, 5 (22%) exceeded this value. This compares favorably with the incidence of 50% reported by Lassnigg during CABG using mild hypothermic CPB [31].
There are a few limitations of the present study which deserve mention. As near infrared spectroscopy is used here in the context of off-pump coronary surgery, our data at the moment stands alone as an observation. This has made difficult a validating comparison with the literature, which is mostly in the context of vascular surgery [27, 30] and conventional coronary surgery [31]. This highlights the need for further studies to validate both NIRS and its application in OPCAB surgery.
In conclusion, this study shows that grafting of the LAD on the beating heart is responsible for changes in cerebral cortical oxygenation, which persist early after returning the heart to its natural position. Grafting of the Cx and PDA only result in transient reversible changes. Trendelenburg positioning and right lateral tilting of the operating table during grafting of lateral and posterior wall might have a protective role in preventing cerebral cortical ischemia. Further studies are needed to assess the clinical importance of these observations.
Acknowledgments
We wish to thank Hamamatsu Photonics, Ltd, UK, for loaning us a NIRO 300 near infrared spectroscope to carry out this study.
References
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  J. Vedin, H. Nyman, A. Ericsson, S. Hylander, and J. Vaage Cognitive function after on or off pump coronary artery bypass grafting. Eur. J. Cardiothorac. Surg., August 1, 2006; 30(2): 305 - 310. [Abstract] [Full Text] [PDF]
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