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Anesth Analg 2003;97:851-856
© 2003 International Anesthesia Research Society

NEUROSURGICAL ANESTHESIA

Measuring Cerebral Oxygenation During Normobaric Hyperoxia: A Comparison of Tissue Microprobes, Near-Infrared Spectroscopy, and Jugular Venous Oximetry in Head Injury

Andrew D. McLeod, FRCA*, Farrell Igielman, FRCA*, Clare Elwell, PhD{dagger}, Mark Cope, PhD{dagger}, and Martin Smith, FRCA*

Departments of *Neuroanaesthesia and {dagger}Medical Physics & Bioengineering, The National Hospital for Neurology and Neurosurgery, University College London Hospitals & Centre for Anaesthesia, UCL, London, United Kingdom

Address correspondence and reprint requests to M. Smith, FRCA, Department of Neuroanaesthesia, Box 30, The National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK. Address e-mail to martin.smith{at}uclh.org


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
We measured simultaneous changes in jugular venous oxygen saturation, brain tissue oxygen tension, and cerebral tissue oxygen index by using near-infrared spectroscopy during normobaric hyperoxygenation in eight severely brain-injured patients. Patients were ventilated at their baseline fraction of inspired oxygen (FIO2), followed by stepped changes in FIO2 to 1.0, 0.6, and 0.02–0.05 less than baseline. There was an increase (P < 0.01) in jugular venous saturation (mean ± SD) from a baseline value of 79% ± 7% to 89% ± 6% and 84% ± 8% at an FIO2 of 1.0 and 0.6, respectively. The changes in brain tissue oxygen tension were from a baseline of 30 ± 5 mm Hg to 147 ± 36 mm Hg and 63 ± 6 mm Hg at an FIO2 of 1.0 and 0.6, respectively (P < 0.01). The baseline tissue oxygen index was 78% ± 3%, and this increased to 83% ± 5% and 80% ± 4% at an FIO2 of 1.0 and 0.6, respectively. There was a reduction (P < 0.05) in tissue oxygen index to 76.2% ± 3.0% when the FIO2 was reduced to less than baseline. The changes in the three variables followed similar patterns but varied in their degree and speed of response. During brain injury, FIO2 affects measured variables of cerebral oxygenation.

IMPLICATIONS: We compared simultaneous measurements of jugular venous saturation, brain tissue oxygen tension, and cerebral tissue oxygen index during normobaric hyperoxia in brain-injured patients. PaO2 influences the output of monitors of cerebral oxygenation, but this does not necessarily equate to improved brain oxygenation.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Monitoring cerebral oxygenation at the bedside is difficult in head-injured patients, and it is unclear which method represents the most valid estimate of the balance between cerebral oxygen delivery and demand. There are also wide differences in regional cerebral blood flow and metabolism after brain injury, and the position of a sensor in the brain is crucial in determining the output from its monitor (1). Global measures of cerebral oxygenation, such as jugular venous saturation (SjO2), may miss important regional changes (1). Thus, there is interest in alternative methods. Direct tissue probe measurement of brain oxygen tension (PbrO2) has been shown to be feasible and comparatively safe (2,3), but this is an invasive technique that is associated with a degree of technical difficulty. Furthermore, PbrO2 is a highly focal measure, and changes in local brain tissue PO2 may not be reflected in global measures of cerebral oxygenation. Near-infrared spectroscopy (NIRS) has also been used to measure cerebral hemodynamics and oxygenation (4). NIRS systems to date have predominantly displayed variables—such as changes in oxygenated and deoxygenated hemoglobin concentrations—that are unfamiliar to clinicians. However, recent developments in NIRS technology have seen the advent of instruments that display a measure of absolute cerebral saturation in an attempt to improve user-friendliness and aid clinical decision making. The NIRO 300 (Hamamatsu Photonics, Hamamatsu City, Japan) measures cerebral tissue oxygenation and returns a single numerator: the tissue oxygenation index (TOI) (5). However, these three monitoring techniques measure different physiological variables and may therefore respond differently to any given change in cerebral oxygenation status. The aim of this study was to compare the influence of normobaric arterial hyperoxia on SjO2, PbrO2, and TOI.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
After institutional ethics committee approval and written, informed consent from the next of kin, eight adult patients with severe closed traumatic brain injury (TBI) were studied. Patients with a baseline fraction of inspired oxygen (FIO2) >0.4 or those who required cardiovascular support with large doses of more than one vasopressor or inotrope were excluded from the study. All eight patients were sedated with IV propofol and fentanyl. The lungs were mechanically ventilated to maintain PaCO2 at 34–38 mm Hg. The patients received routine, protocol-driven management to limit increases in intracranial pressure (ICP) and maintain cerebral perfusion pressure >70 mm Hg. Measures to prevent or treat pyrexia were also provided. The following monitoring was established as part of the patient’s routine clinical management. ICP was monitored continuously by using an intraparenchymal microsensor (Codman, Randolph, MA). SjO2 was measured with a standard optical catheter (Opticath; Abbott Laboratories, Chicago, IL) sited in the bulb of the right internal jugular vein. Location of the catheter tip was confirmed by lateral cervical spine radiograph, and optically obtained values were calibrated against cooximeter readings (Radiometer ABL 520; Radiometer Ltd., Copenhagen, Denmark) of directly aspirated samples. A multiparameter sensor (Neurotrend®; Codman) was inserted for continuous monitoring of PbrO2 and brain temperature. This was sited in the frontal cortex on the same side as the ICP monitor and distant from any area of contusion. The sensor contains two modified optical fibers for pH and PCO2 measurements, a Clarke electrode for PO2, and a thermocouple to measure brain temperature (2,3). The sensor was calibrated before insertion by using an automated precision gas sequence, and an in vivo equilibration period of at least 4 h was allowed. PbrO2 was corrected for brain temperature. Correct location in the cerebral cortex was subsequently confirmed by computed tomography. In addition, invasive arterial blood pressure, pulse oximetry (SpO2), and electrocardiogram were recorded in all patients.

During the study period, TOI was measured with a NIRO 300 spectrophotometer, which uses laser-emitting diodes to generate light at four different wavelengths (typically 775, 810, 850, and 910 nm). It uses the technique of spatially resolved spectroscopy and uses multiple, closely spaced detectors to measure light attenuation as a function of source-detector separation. From these measurements it is possible to decouple the absorption and scattering coefficients and combine this with an estimation of the wavelength dependence of light scattering. The result is a measurement of scaled absolute hemoglobin concentrations, i.e., the relative proportions of oxyhemoglobin (HbO2) and hemoglobin (HHb), from which tissue oxygen saturation is computed (5). TOI is the ratio of oxygenated to total tissue hemoglobin concentration and can be expressed as follows:


In addition to measurement of TOI, the NIRO 300 is able to measure changes from baseline of cerebral oxygenated and deoxygenated hemoglobin concentrations by using a modification of the Beer-Lambert law (6). Changes in total cerebral hemoglobin (HbT) concentration were converted to changes in cerebral blood volume (CBV) by using a previously described relationship (7) and a differential pathlength factor of 6.26 (8). The HbT concentration changes in proportion to CBV if the hemoglobin concentration (Hb) and the cerebral large to small vessel hematocrit ratio remain constant during the measurement period (7).


Although this technique does not allow measurement of absolute CBV, its advantage lies in the ability to make real-time measurements of changes in CBV. The NIRS optodes (transmitting and receiving devices) were placed on the scalp over the frontal region, anterior to the tissue probe and approximately 4 cm above the supraorbital ridge. A purposely designed holder ensured a constant interoptode separation of 40 mm and adequate light shielding.

At the start of the study, the lungs were ventilated at baseline FIO2 for 10 min, after which the FIO2 was increased to 1.0 for 30 min and then decreased to 0.6 for a further 30 min. Finally, the FIO2 was reduced to 2%–5% less than baseline (to produce a reduction in SpO2 of not more than 2%) for 30 min. Patients were then returned to their baseline FIO2 value, and the study period ended. All other ventilator settings remained unchanged during the study. The 10 min baseline period and the final 10 min period of each FIO2 sequence was used for data analysis (the stable period), allowing equilibration of physiological variables during the first 20 min at each new FIO2. The following data were recorded onto a computer at 1-s intervals throughout the study: PbrO2, TOI, changes in oxygenated and deoxygenated Hb, and continuous values for SjO2. During each stable period, the following variables were recorded manually at 1-min intervals; ICP, mean arterial blood pressure (MAP), heart rate, and SpO2. At the start and finish of each stable period, arterial blood was drawn for blood gas analysis; in the middle of each equilibrating period, a sample of blood was aspirated from the jugular venous catheter, and the optical catheter was recalibrated if necessary.

By using specially written software, the continuous data were converted into spreadsheet format (Excel; Microsoft Corp., Redmond, WA) and the intermittent values were later incorporated manually into the spreadsheet. For all variables, the mean value during each stable period was calculated and used as the summary measure.

Oxygen reactivity was calculated as the change in PbrO2 in response to changes in PaO2 according to a previously described equation (2).



Changes in each variable of cerebral oxygenation were compared with the respective baseline values by using a paired Student’s t-test. A Bonferroni correction factor was applied, and significance was accepted at P < 0.05. Values are presented as mean ± standard deviation.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
All eight patients were male, were aged 22–44 yr, and had a postresuscitation Glasgow Coma Scale score <8. Seven patients had diffuse brain injury, and one had undergone surgical evacuation of a subdural hematoma before the study. No complications of invasive monitoring were observed. There were no changes in MAP or brain temperature during the study protocol (Table 1). The changes in PaO2, PaCO2, and SpO2 values during the four levels of oxygenation are shown in Table 1.


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  		Table 1. Physiologic Values at Respective Fraction of Fraction of Inspired Oxygen (FiO2) Trials
 
Table 2 presents summary values for TOI, PbrO2, and SjO2 for all patients during the four phases of oxygenation. Figure 1 shows the changes in TOI, PbrO2, and SjO2 in one patient during the study period. Similar patterns of change were seen in all patients. PbrO2 changed over a proportionately larger range and took longer to attain steady-state than SjO2 or TOI. Oxygen reactivity was 8.30% ± 2.68%, with a range of values from 3.92% to 11.69%.


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  		Table 2. Values for Each Measure of Cerebral Oxygenation at Four Different Fraction of Inspired Concentration (FiO2) Values
 


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  		Figure 1. The figure shows a simultaneous recording of three measures of cerebral oxygenation during four inspired oxygen fractions (FIO2) in a single patient. The pattern of changes was similar in all patients. Tissue oxygenation index (TOI) and brain tissue oxygen tension (PbrO2) are shown as real-time continuous traces. Jugular venous saturation (SjO2) is shown as a mean value for the stable period at each FIO2 because the noise from the continuous signal obscured the other traces.

 
CBV changes are shown in Table 3. A decrease in CBV (P < 0.05) was seen during hyperoxia; this was associated with a decrease in ICP (P < 0.05), followed by a rebound (but not statistically significant) increase in both during mild hypoxia. Cerebral deoxygenated hemoglobin concentration decreased significantly during hyperoxia (FIO2 = 1.0 and 0.6) and was accompanied by a more modest increase in oxygenated hemoglobin concentration.


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  		Table 3. Cerebral Blood Volume (CBV), Intracranial Pressure (ICP), and Changes in Cerebral Oxygenated Hemoglobin ({Delta}[HbO2]), Deoxygenated Hemoglobin ({Delta}[Hb]), and Total Hemoglobin ({Delta}[HbT]) Concentrations at Respective Fraction of Inspired Oxygen (FiO2) Values
 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
This study demonstrates that alterations in PaO2 are associated with changes in the three measured variables of cerebral oxygenation. PbrO2 increased significantly from baseline values during hyperoxia, but the sensor exhibited a time lag in reaching steady-state. This may have reflected equilibration of local oxygen gradients rather than the sensor’s response time, which is reported as 70 seconds in vitro for a 0% to 90% change (9). TOI and SjO2 showed modest, but statistically significant, increases from baseline during hyperoxia, and this was associated with a small but consistent decrease in CBV and ICP. There was little time lag in TOI and SjO2 reaching steady-state at each new FIO2 level. There were no other physiological changes in any patient during the study protocol (such as cardiovascular variables, brain temperature, PaCO2, or depth of sedation) that could potentially have caused confounding changes in cerebral hemodynamics and oxygenation.

The degree of hypoxia we induced was very slight, so it is difficult to draw clear conclusions about the response of the monitors to reductions in PaO2. Furthermore, our results for this period may have been influenced by the previous periods of hyperoxygenation. This hypothesis could be further investigated by conducting alternative sequences of oxygenation, but clearly it would be unethical to induce more extreme or prolonged reductions in PaO2 in brain-injured patients. It is therefore likely that such information will only be obtained from animal studies.

The effect of hyperoxia on cerebral oxygenation has been noted previously (2,10,11) but not described in a simultaneous comparison of these three monitors. Similar comparisons have been made during different clinical circumstances, but all such studies are problematic (1,12). Each monitor uses a different physical principal and measures a distinct physiological variable. For this reason, we chose to make a simple statistical summary of changes from baseline, rather than attempting to establish spurious correlations between the monitors.

Jugular venous oximetry is widely used to obtain information about the adequacy of cerebral oxygenation after head injury on a continuous basis at the bedside (13,14). However, it is a global measure and can miss important episodes of regional ischemia (1). In our study, the baseline value for SjO2 was high, and this may have been related to hyperemia. Increased SjO2 values are usually considered to represent excess ("luxury") perfusion or decreased cerebral oxygen consumption (13). However, increases of SjO2 occur in almost 20% of patients after head injury, and it has recently been suggested that this is a heterogeneous condition that cannot automatically be associated with hyperemia (15). Notwithstanding the increased baseline level, SjO2 increased in each patient during the period of arterial hyperoxia, and this finding has been described previously (10). However, inferring that the increase in SjO2 equates with increased cerebral oxygenation may not be valid, because it could equally imply greater arteriovenous shunting secondary to vasoconstriction or maldistribution of blood flow (16).

Microprobes inserted directly into brain tissue can record a value for tissue oxygen tension, and normal values of PbrO2 ranging from 25 to 45 mm Hg have been reported (2,17). Reductions in PbrO2 have the potential to correlate with adverse events and poor outcome after brain injury (2,18,19), but the absolute value remains of uncertain significance. Oxygen metabolism within the brain is heterogeneous, and different values have been recorded within a small area (20). Furthermore, probes inserted within or outside areas of focal contusion after brain injury provide widely varying information (1). The effects of probe insertion itself must be also considered, and local vasoconstriction may account for low initial values (21). In common with other studies, our study protocol allowed a four-hour "run-in" period to minimize these effects. More importantly, though, tissue PO2 remains a physiologically vague concept, and the exact relationship between intracellular PO2 and "tissue" PO2 remains undefined. The relationship between arterial PaO2 and PbrO2 has previously been noted (2,11) and described in terms of oxygen reactivity (2). We found values of oxygen reactivity comparable to those of other studies, supporting the observation that PbrO2, as recorded by a tissue microprobe, is strongly influenced by the prevailing PaO2. This effect could be greatest in the injured brain, and other values—such as PbrCO2 or pH—could prove to be more useful indicators of ischemia.

NIRS allows noninvasive assessment of cerebral hemodynamics and oxygenation (4,6). The NIRO 300 derives an absolute value for TOI (5) that represents all cerebral blood compartments, with the exception of the larger vessels, and is a relatively focal measurement. In this study, the increases in TOI during hyperoxygenation occurred principally through decreases in cerebral deoxygenated hemoglobin concentration; only modest increases were observed in the oxygenated hemoglobin concentration. This implies a reduction in oxygen extraction by the brain, perhaps occurring as a result of an increase in cerebral oxygen delivery. Similar conclusions have been reached by using functional magnetic resonance imaging measurements (22). CBV was reduced during hyperoxia, which is consistent with oxygen’s known actions as a vasoconstrictor and its propensity to reduce ICP (23). The clinical use of NIRS remains limited by potential sources of error that include contamination of the signal by the extracerebral circulation (principally the scalp), extraneous light, and the presence of extravascular blood, e.g., subarachnoid or subdural hemorrhage. With use of the NIRO 300 to investigate cerebral oxygenation changes during carotid surgery, the sensitivity of TOI to intracranial changes was 87.5%, with a specificity of 100% (24). In contrast, the sensitivity and specificity to extracranial changes were 0%, suggesting that TOI, as measured by the NIRO 300, is able to measure changes in cerebral tissue oxygenation. Older NIRS technologies have been used to monitor cerebral oxygenation in adults in various clinical settings and as part of a multimodality monitoring system in head injury (4,25,26). However, the application of spatially resolved spectroscopy and the validity of TOI have been described only in healthy volunteers (27) and in the context of carotid surgery (24). The findings from our study suggest that TOI might be a useful adjunct for monitoring cerebral oxygenation in the setting of TBI, but further studies are required to validate its use in this context.

The term cerebral oxygenation is often used loosely to mean different things. For example, SjO2, PbrO2, and TOI all measure an aspect of cerebral oxygenation, but their measurements represent different physiological variables from different areas of the brain. Changes in FIO2 resulted in varying responses in SjO2, PbrO2, and TOI, and this is to be expected because the three monitors measure different things. PbrO2 measures tissue oxygen tension, which may be directly related to FIO2. SjO2, however, measures saturation, which does not have a linear relationship with FIO2. The relationship between TOI and FIO2 has not been quantified, but, because it is also a saturation measurement, it might be expected to follow the changes in SjO2 more closely than those in PbrO2. The real-time changes in the three variables of cerebral oxygenation measured in this study suggest that this is the case.

Hyperoxia causes cerebral vasoconstriction, reduces cerebral blood flow, and, at hyperbaric pressures, has other effects on cerebral metabolism (28). Hyperbaric oxygen therapy has been applied to head-injured patients and was associated with improved mortality, but there was no increase in the number of surviving patients with a favorable outcome (29). However, a study using cerebral microdialysis showed favorable changes in brain lactate levels during normobaric hyperoxia (11). By conventional understanding, increasing PaO2 under normobaric conditions cannot greatly increase cerebral oxygen delivery. Experiments in a porcine model of cerebral ischemia demonstrated that inadequate oxygen delivery is reflected in small values of PbrO2 but that manipulating tissue oxygen tension (by deliberate hyperoxia) does not conversely improve cerebral oxygen delivery (30). It is possible that TOI, which measures the oxygen content of all cerebral blood compartments, might represent a more useful measure of cerebral oxygenation than PbrO2 in these circumstances. Its more rapid response time is also advantageous.

This study demonstrates that, whatever variable of cerebral oxygenation is measured, altering FIO2 will profoundly affect the results. Multivariable monitoring provides a more complete picture of cerebral oxygenation after head injury than individual techniques, but changes in systemic physiology (such as PaO2) must be considered when results from cerebral oxygenation monitors are interpreted. It cannot be assumed that an improvement in a measured variable of cerebral oxygenation necessarily equates to an actual improvement in brain oxygenation. The effects of hyperoxia on the output from the monitors must be distinguished from its complex actions on the brain.


   Acknowledgments
 
The authors are grateful to Hamamatsu Photonics for loan of the NIRO 300 and to Codman UK for the loan of the Neurotrend.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication April 3, 2003.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press