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Ann Thorac Surg 1996;61:930-934
© 1996 The Society of Thoracic Surgeons


Original Articles: Cardiovascular

Cerebral Oxygenation Measured by Near-Infrared Spectroscopy: Comparison With Jugular Bulb Oximetry

Piers E. F. Daubeney, MBBS, Sally N. Pilkington, MBBS, Ellen Janke, MD, Gareth A. Charlton, MBBCh, David C. Smith, Bmbs, Steven A. Webber, MBChB

Wessex Cardiothoracic Centre, Southampton General Hospital, Southampton, United Kingdom

Accepted for publication November 17, 1995.


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Near-infrared spectroscopy is a potential tool for measuring adequacy of cerebral oxygenation during cardiac operations. The cerebral microcirculation is predominantly venous (by volume) and therefore regional cerebral oxygenation measured by near-infrared spectroscopy should reflect jugular bulb venous saturations.

Methods. We compared simultaneous regional cerebral oxygenation and jugular bulb venous saturation measurements in 40 children (median age, 4.5 years; range, 2 weeks to 14.5 years) in the cardiac catheter laboratory (n = 29) and during cardiac operations (n = 11).

Results. For all patients combined the correlation between regional cerebral oxygenation and jugular bulb venous saturation was 0.69 (p < 0.0001) and was similar for the two groups. For individual children undergoing cardiac operations excellent correlations were obtained (r = 0.78 to 0.96; median, 0.91). However, at low values of jugular bulb venous saturation, regional cerebral oxygenation tended to run high, whereas the converse was true for high values of jugular bulb venous saturation.

Conclusions. These findings suggest that near-infrared spectroscopy may be a useful tool for assessing intravascular cerebral oxygenation during pediatric cardiac operations. Prospective studies of neurologic outcome will be required to establish the value of this technique for assessing the adequacy of cerebral protection.


    Introduction
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
See also page 934.

Imbalance between cerebral oxygen supply and demand is thought to play an important role in the development of neurologic injury after pediatric cardiac operations [1]. Monitoring of cerebral oxygenation may help predict when patients are at risk of the development of such injury. Recently, measurement of jugular bulb saturations has been used during cardiac operations for the purpose of assessing the global cerebral oxygen supply/demand relationship [2, 3]. Near-infrared spectroscopy [4] is a potential tool for the noninvasive and continuous assessment of cerebral oxygenation during cardiac operations, particularly during hypothermic circulatory arrest when other modalities are not available [5, 6]. In this study we compared regional cerebral oxygen saturations (rSO2) measured by near-infrared spectroscopy with jugular bulb venous oxygen saturations (SjO2) in children with congenital heart disease undergoing cardiac catheterization or cardiac operations.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
After ethical committee approval (September 1993) and informed parental consent, 40 children were studied. The median age was 4.5 years (range, 2 weeks to 14.5 years). There were 26 boys and 14 girls. Median head circumference was 50 cm; range, 35 to 58 cm; and weight range, 3.3 to 75.1 kg. Twenty-nine children undergoing routine cardiac catheterization were studied in the cardiac catheterization laboratory. Their diagnoses were diverse and included acyanotic and cyanotic forms of congenital heart disease. Eleven children undergoing palliative or reparative cardiac operations under cardiopulmonary bypass were studied in the operating theater (Table 1Go).


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Table 1. . Characteristics of Patients Undergoing Cardiac Operations
 
In the catheter laboratory all patients received general anesthesia using a standard technique involving premedication with 0.5 mL/kg of a mixture containing trimeprazine (3 mg/mL), atropine (60 µg/mL), and morphine (1 mg/mL), intravenous induction with 3 to 5 mg/kg thiopentone, and paralysis with vecuronium or pancuronium. Maintenance was with isoflurane (0.5% to 1%) in nitrous oxide and oxygen. Ventilation was adjusted to maintain normocarbia, as assessed by continuous end-tidal CO2 monitoring and intermittent arterial blood gas analysis. For cardiac operations the only additions were either morphine or fentanyl for analgesia. Cardiopulmonary bypass used a nonpulsatile roller pump (Stockert, Munich, Germany) and membrane oxygenator (Sorin, Mirandola, Italy). Standard pump flow rates were 100 to 120 mL•kg-1•min-1, although in selected patients periods of low-flow bypass were employed. Alpha-stat management of acid-base status was used during cardiopulmonary bypass. For circulatory arrest, patients were cooled to approximately 16°C before venous exsanguination was performed.

Near-infrared monitoring used the INVOS 3100 cerebral oximeter (Somanetics Corp, Troy, MI). In brief, this measures intracerebral oxygen saturation by spectroscopy of reflected near-infrared light. Because the cerebral microcirculation contains arterial, venous, and capillary components, the rSO2 represents a weighted average assuming the venous component to be predominant (estimated as 75% by volume) [7]. The sensor comprises a near-infrared light transmitter and two photodetectors (optodes) spaced 3 and 4 cm from the infrared source. This arrangement allows spatial resolution because the optode nearest the light source receives a signal from light that has traveled in an arc through superficial tissues, whereas the more distant optode receives light that has passed through superficial and deeper tissues. ``Subtraction'' of the two signals allows calculation of oxygen saturation of hemoglobin from cerebral tissue while minimizing ``contamination'' from superficial (extracerebral) sources [8, 9]. The light source and optodes are contained within a flexible adhesive pad, which was placed over the forehead lateral to the midline to avoid the superior sagittal sinus and at least 2 cm above the eyebrows to avoid the frontal sinus.

In the cardiac catheter laboratory the jugular bulb was entered under fluoroscopic guidance from a femoral vein approach. Blood samples were taken and the oxygen saturation measured using a calibrated OSM 2 Haemoximeter (Radiometer, Copenhagen, Denmark). Simultaneous systemic arterial saturations were obtained along with rSO2 readings over a wide range of inspired oxygen concentrations. Blood samples and rSO2 readings were obtained during steady state conditions at least 5 minutes after any change in ventilator settings.

For studies performed during cardiac operations the internal jugular vein was cannulated in a retrograde fashion with a 20-gauge cannula (Vygon, Ecouen, France) using a percutaneous technique. The catheter was advanced into the jugular bulb. Jugular bulb venous saturations were measured as above and compared with the concurrent rSO2 reading. Repeated jugular venous sampling was performed in the period before bypass, during bypass, and after bypass. Samples were not drawn during hypothermic circulatory arrest. Sampling was avoided at the time of acute interventions (eg, change in bypass flow rates). Samples were discarded if fluctuations in rSO2 of more than 1% occurred in the 2-minute period immediately before or after sampling.

The relationship between rSO2 and SjO2 was explored using simple linear regression analysis and a bias plot of the difference between rSO2 and SjO2 against SjO2.


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The data were analyzed for all patients combined, for differing clinical setting (eg, catheter laboratory or operating theater), for differing ages, and for individual patients (Table 2Go). For all data points (n = 147) for all patients combined, rSO2 was significantly correlated with SjO2 (rSO2 = 0.5SjO2 + 34.1; r = 0.69; p < 0.0001) (Fig 1Go). This relationship was similar for the following groups analyzed separately: catheter laboratory studies, prebypass studies, and catheter laboratory combined with prebypass studies. The latter two groups were combined because patients in these two categories were in a similar clinical setting, ie, general anesthesia under normothermia or mild hypothermia. To ensure independence of data points, the data were reanalyzed using only the first sample from each patient. This did not alter the relationship between rSO2 and SjO2. During cardiopulmonary bypass the regression line had a more shallow slope and greater intercept but similar correlation coefficient (see Table 2Go). Stratifying the patients into infants (<=1 year) and children (>1 year) showed that the correlation between rSO2 and SjO2 was much closer in infants (r = 0.85; p < 0.0001) than in children (r = 0.57; p < 0.0001) (see Table 2Go).


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Table 2. . Relationship Between Regional Oxygen Saturation of the Brain (y) and Jugular Venous Bulb Oxygen Saturation (x) for Patients in the Categories Listed
 


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Fig 1. . Correlation between regional cerebral oxygen saturation (rSO2) and jugular bulb oxygen saturation (SjO2) for all patients studied both in the cardiac catheterization laboratory and during open heart operation. Mean and 95% confidence limits around mean are shown.

 
For 10 of the 11 children studied during cardiac operations, the correlation between rSO2 and SjO2 in the individual patient was much closer than for all patients combined (median r = 0.91; range, 0.78 to 0.96) (Fig 2Go). However, there was a wide range of slopes (0.35 to 0.85) for the line of regression. Data were not analyzed for 1 patient in whom there was only minimal variation in both SjO2 and rSO2 throughout the procedure. A bias plot of the difference between rSO2 and SjO2 against SjO2 is shown in Figure 3Go. Mean difference between rSO2 and SjO2 was -0.7% (standard deviation, 10.1%). However, for high values of SjO2, rSO2 tends to run low, whereas the converse is true for low levels of SjO2.






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Fig 2. . Correlation between regional cerebral oxygen saturation (rSO2) and jugular bulb oxygen saturation (SjO2) in 4 representative patients undergoing repair of congenital heart defects. Mean and 95% confidence limits around mean are shown. (AVSD = atrioventricular septal defect.)

 


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Fig 3. . Bias plot of the difference between regional cerebral oxygen saturation (rSO2) and jugular bulb oxygen saturation (SjO2) against SjO2 for all patients combined. Solid horizontal line represents mean difference.

 

    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Over the last two decades substantial advances have been made in the surgical management of most forms of congenital heart disease [10, 11]. Although dramatic reductions in surgical mortality have been achieved, neurologic sequelae remain a frequent and potentially devastating complication of open heart operations [10, 11]. Although such injury is almost certainly multifactorial in origin [1, 11], imbalance between cerebral oxygen supply and demand is likely to be an important determinant of neurologic outcome [1]. This has led to a search for tools that can help assess the cerebral oxygen supply/demand relationship [12]. During cardiopulmonary bypass, cerebral blood supply is fully saturated with oxygen, and assessment of SjO2 provides a global estimate of cerebral oxygen extraction [2, 3]. Near-infrared spectroscopy is a tool that has the potential to provide similar but continuous, noninvasive, and safe (covered by European standard BS EN 60825) information about cerebral oxygenation status. Although estimates of rSO2 include arterial and capillary components, the largest contribution is considered to be venous, which has been estimated to represent 75% of the cerebral blood volume [7]. Thus changes in SjO2 should be paralleled by changes in rSO2, although close agreement between the two parameters would not necessarily be expected as different entities are being measured. We therefore sought to explore the relationship between SjO2 and rSO2 as measured by near-infrared spectroscopy (INVOS 3100) to assess its potential for use during pediatric cardiac operations.

We have shown a reasonable correlation between rSO2 and SjO2 (r = 0.69) when all patient data were combined across different clinical settings. The strength of this relationship was similar in different clinical settings (eg, general anesthesia for cardiac catheterization, before and during cardiopulmonary bypass). The relationship was stronger in infants compared with children, and when individual patients were examined, the correlation between rSO2 and SjO2 was even closer (median r = 0.91), although the relationship between the two variables (as defined by linear regression analysis) varied considerably between patients. In particular the line of regression showed a wide range of gradients. This suggests that it may not be possible to predict absolute SjO2s for any given patient based solely on rSO2 readings. Near-infrared spectroscopy, using the INVOS 3100 cerebral oximeter, may be most useful for indicating trends in cerebral oxygenation status in individual children.

It should also be noted that the magnitude and direction of the difference between rSO2 and SjO2 varied with the absolute value of SjO2. In practical terms, for high values of SjO2, rSO2 runs low, whereas at low values it runs high. Thus, severe desaturation of jugular venous return might not always be recognized. Conversely, it may be hard to be sure when cerebral metabolism has nearly ceased during profound hypothermia as rSO2 values rarely rose to more than 90%. In addition it should be noted that intravascular oxygenation may not always accurately reflect intracellular oxygen availability. Du Plessis and colleagues [13] recently described a dissociation of cerebral intravascular and mitochondrial oxygenation by comparing changes in hemoglobin O2 saturation to changes in oxidized cytochrome aa3. Thus measurement of cerebral intravascular oxygenation alone may be an inadequate method for assessing adequacy of cerebral protection during periods of decreased cerebral blood flow or circulatory arrest.

The reasons for the variable relationship between rSO2 and SjO2 between patients (despite the excellent correlation in individual patients) are not entirely clear. The monitor was designed for adult use, and technical adjustments for differing age groups may be required in view of the differing head shapes and thickness of extracerebral (superficial) tissues. Some concern has been expressed that in adults, rSO2 as measured by the INVOS 3100 is excessively contaminated by signal from blood in the extracerebral tissues [14]. Spatial resolution is likely to be achieved more easily in the pediatric age group, due to decreased thickness of the superficial extracerebral tissues [14]. This might explain the closer relationship between rSO2 and SjO2 in infants as compared with older children in the current study. Furthermore, the device assumes a constant optical density and photon path length, an assumption that may not be valid across the wide pediatric age range and for all clinical conditions. It should also be noted that the vascular composition of the brain is likely to change during cardiopulmonary bypass and circulatory arrest. As rSO2 depends on the weighted contributions of the differing vascular compartments, alterations in the latter will affect the relationship between rSO2 and SjO2.

Our observations suggest that in infants and children, near-infrared spectroscopy is a potentially useful tool for monitoring trends in cerebral intravascular oxygenation and may become an important adjunct for the monitoring of infants and children undergoing cardiac operations. At the present time there is no ``gold standard'' for measurement of cerebral oxygenation. Thus, the clinical utility of this technique will only be established if prospective clinical studies confirm the ability of near-infrared spectroscopy to predict and prevent adverse neurologic sequelae during pediatric cardiac operations.


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Piers E. F. Daubeney, MBBS, is supported by the Wessex Cardiac Trust.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Greeley WJ, Kern FH, Mault JR, Skaryak LA, Ungerleider RM. Mechanisms of injury and methods of protection of the brain during cardiac surgery in neonates and infants. Cardiol Young 1993;3:317–30.
  2. Nakajima T, Kuro M, Hayashi Y, Kitaguchi K, Uchida O, Takaki O. Clinical evaluation of cerebral oxygen balance during cardiopulmonary bypass: on-line continuous monitoring of jugular venous oxyhemoglobin saturation. Anesth Analg 1992;74:630–5.[Abstract/Free Full Text]
  3. Kern FH, Jonas RA, Mayer JE Jr, Hanley FL, Castañeda AR, Hickey PR. Temperature monitoring during CPB in infants: does it predict efficient brain cooling? Ann Thorac Surg 1992;54:749–54.[Abstract]
  4. Jobsis FF. Non-invasive infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science 1977;198:1264–7.[Abstract/Free Full Text]
  5. Kurth CD, Steven JM, Nicolson SC, Chance B, Delivoria-Papadopoulos M. Kinetics of cerebral deoxygenation during deep hypothermic circulatory arrest in neonates. Anesthesiology 1992;77:656–61.[Medline]
  6. Fallon P, Roberts I, Kirkham FJ, et al. Cerebral hemodynamics during cardiopulmonary bypass in children using near-infrared spectroscopy. Ann Thorac Surg 1993;56:1473–7.[Abstract]
  7. Mchedlishvili GI. Arterial behavior and blood circulation in the brain. New York: Plenum, 1986:55–60.
  8. Williams IM, Vohra R, Farrell A, Picton AJ, Mortimer AJ, McCollum CN. Cerebral oxygen saturation, transcranial Doppler ultrasonography and stump pressure in carotid surgery. Br J Surg 1994;81:960–4.[Medline]
  9. McCormick PW, Stewart M, Goetting MG, Dujovny M, Lewis G, Ausman JI. Noninvasive cerebral optical spectroscopy for monitoring cerebral oxygen delivery and hemodynamics. Crit Care Med 1991;19:89–97.[Medline]
  10. Ferry PC. Neurologic sequelae of cardiac surgery in children. Am J Dis Child 1987;141:309–12.[Abstract/Free Full Text]
  11. Wernovsky G, Jonas RA, Hickey PR, du Plessis AJ, Newburger JW. Clinical neurologic and developmental studies after cardiac surgery utilizing hypothermic circulatory arrest and cardiopulmonary bypass. Cardiol Young 1993;3:308–16.
  12. Kern FH, Greeley WJ, Ungerleider RM. The assessment of cerebral function during paediatric cardiopulmonary bypass. Perfusion 1993;8:63–70.[Free Full Text]
  13. Du Plessis AJ, Newburger J, Jonas RA, et al. Cerebral oxygen supply and utilization during infant cardiac surgery. Ann Neurol 1995;37:488–97.[Medline]
  14. Germon TJ, Kane NM, Manara AR, Nelson RJ. Near-infrared spectroscopy in adults: effects of extracranial ischaemia and intracranial hypoxia on estimation of cerebral oxygenation. Br J Anaesth 1994;73:503–6.[Abstract/Free Full Text]

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