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Anesth Analg 2001;92:1370-1376
© 2001 International Anesthesia Research Society

CARDIOVASCULAR ANESTHESIA

The Association of High Jugular Bulb Venous Oxygen Saturation with Cognitive Decline After Hypothermic Cardiopulmonary Bypass

Kenji Yoshitani, MD, Masahiko Kawaguchi, MD, Nobuko Sugiyama, MD, Masatoshi Sugiyama, MD, Satoki Inoue, MD, Takanori Sakamoto, MD, Katsuyasu Kitaguchi, MD, and Hitoshi Furuya, MD

Department of Anesthesiology, Nara Medical University, Nara, Japan

Address correspondence and reprint requests to Kenji Yoshitani, MD, Department of Anesthesiology, Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634-8522, Japan. Address e-mail to nkenji{at}mva.biglobe.ne.jp


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
This study was conducted to investigate whether jugular bulb venous oxygen saturation (SjVO2) predicted cognitive decline after cardiac surgery with hypothermic cardiopulmonary bypass (CPB). We studied 35 patients undergoing cardiac surgery. After the induction of anesthesia, a 5.5F fiberoptic oximetry catheter was retrogradely inserted into the jugular bulb, and SjVO2 and other cerebral oxygenation variables were analyzed before, during, and after CPB. At each point, an oxyhemoglobin dissociation curve was drawn, and the P50 value of jugular bulb venous blood was calculated by computer analysis. Cognitive function was assessed with the revised version of Hasegawa’s Dementia Scale and the Benton Revised Visual Retention Test before and early after the operation. In 15 patients (the Decline group), cognitive function was declined after surgery, whereas it remained unchanged in 20 patients (the Normal group). SjVO2 was significantly higher and cerebral oxygen extraction was significantly lower before and during CPB in the Decline group than in the Normal group (P < 0.05). The oxygen pressure at an oxygen saturation of 50% was significantly lower before and after CPB in the Decline group than in the Normal group (P < 0.05). Logistic regression analysis showed that high SjVO2 was a predictor of cognitive decline after cardiac surgery. We conclude that high SjVO2 was associated with cognitive decline after cardiac surgery with hypothermic CPB.

Implications: Jugular bulb venous oxygen desaturation has been suggested as a predictor of cognitive decline after cardiac surgery. However, the clinical value of jugular bulb venous oxygen saturation (SjVO2) may be limited during hypothermic cardiopulmonary bypass (CPB) when oxygen affinity to hemoglobin is increased. This study shows that high SjVO2 before and during hypothermic CPB is a predictor of subsequent cognitive decline.


   Introduction
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 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Neuropsychological dysfunction after cardiac surgery is common and is a significant cause of morbidity. The incidence described in the literature varies between 33% and 83% during the early postoperative period (1–4). It may persist in up to 35% of patients for at least 12 mo (5). Although many attempts have been made to establish predictors of postoperative neuropsychological dysfunction, the etiology of neuropsychological impairment after cardiac surgery remains unsolved (2). Early studies suggested that hypoperfusion or hypotension leading to inadequate cerebral perfusion might be associated with postoperative cognitive dysfunction (3). Two studies with measurement of jugular bulb venous oxygen saturation (SjVO2) directly revealed that oxygen desaturation during rewarming on cardiopulmonary bypass (CPB) was associated with cognitive dysfunction (6,7).

In contrast, it has been suggested that the clinical value of venous oxygen saturation may be limited during episodes of increased oxygen affinity to hemoglobin caused by hypothermia and alkalosis (8). Dexter and Hindman (9) demonstrated that high SjVO2 values might indicate decreased offloading of oxygen from hemoglobin and not necessarily indicate adequate tissue oxygenation. Murkin and Buchan (10) suggested that neurologic outcome might be poorer in patients with higher SjVO2 during hypothermic CPB. Therefore, the role of SjVO2 as a predictor of cognitive dysfunction has been controversial. This study was therefore conducted to investigate whether SjVO2 could be used to predict cognitive decline after cardiac surgery accompanied with hypothermic CPB. In this study, to evaluate the affinity of oxygen to hemoglobin, the oxyhemoglobin dissociation curve (ODC) was drawn, and the oxygen pressure at an oxygen saturation of 50% (P50) value of jugular bulb venous blood was calculated by computer analysis.


   Methods
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 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
After IRB approval, informed consent was obtained from each patient. Thirty-five patients scheduled for elective cardiac surgery with CPB were studied. Patients with a history of cerebrovascular disease or renal disease were excluded from the study.

All patients were premedicated with scopolamine, morphine, and bromazepam 30 min before the induction of anesthesia. Anesthesia was induced with midazolam 0.1 mg/kg, fentanyl 20 µg/kg, and vecuronium 0.15 mg/kg. After the trachea was intubated, the lungs were mechanically ventilated. A cannula was inserted into the left radial artery to monitor arterial blood pressure and to sample the arterial blood for blood gas analysis. A 5.5F fiberoptic oximeter catheter (Opticath; Abbott Laboratories, North Chicago, IL) was also passed to the right jugular bulb retrogradely through the right internal jugular vein for sampling of jugular bulb venous blood. Proper position of the tip of the catheter was radiographically verified. Anesthesia was maintained with continuous infusion of midazolam 0.05 mg · kg-1 · h-1, fentanyl 5 µg · kg-1 · h-1, and vecuronium 0.1 mg · kg-1 · h-1 throughout the operative period. Rectal temperature was continuously monitored (Hewlett-Packard, Palo Alto, CA). The tympanic membrane temperature was also continuously monitored by Mon-a Therm (Mallinckrodt Co., St. Louis, MO).

The CPB circuit was primed with crystalloid, and a nonpulsatile pump flow rate of 2.2 to 2.5 L · min-1 · m-2 was maintained. A membrane oxygenator and a 40-µm arterial line filter were used. PaCO2 uncorrected for temperature was adjusted to normocapnic levels (35 to 40 mm Hg) by varying fresh gas flow to the membrane oxygenator ({alpha}-stat regulation). The target rectal temperature was 28°C. Phenylephrine infusion was used during CPB to maintain mean arterial pressure (MAP) at 50–70 mm Hg.

By use of an ABL505 analyzer (Radiometer, Copenhagen, Denmark), the following variables were measured within 3 min after the simultaneous sampling of arterial and jugular bulb venous blood: arterial and jugular bulb venous partial pressure of carbon dioxide (PaCO2 and PjvCO2, respectively) and oxygen (PaO2 and PjvO2, respectively), pH, hemoglobin (Hb), and arterial and jugular bulb venous oxygen saturation (SaO2 and SjVO2, respectively). To estimate cerebral oxygenation state, arteriojugular venous oxygen content difference (Ca-jvO2) and cerebral oxygen extraction ratio (COER) were calculated with the following equations:

equation


equation


equation


equation


where CaO2 and CjvO2 are the arterial and jugular bulb venous oxygen contents.

Additionally, the ODC was constructed with a personal computer by using the model of Siggaard-Andersen et al. (11), and the P50 of jugular bulb venous blood was calculated. P50 adjusted to patients’ pH, PCO2, and temperature (37°C) was used for the analysis. Hemodynamic variables and arterial and jugular bulb venous blood gas analyses were obtained at the following points: 1) just after the induction of anesthesia; 2) 10 min after the beginning of surgery; 3) at 28°C during stable hypothermic CPB; 4) at 30°C during rewarming; 5) at 34°C during rewarming; 6) at the cessation of CPB; 7) 60 min after the cessation of CPB; and 8) at the end of operation.

Cognitive function was assessed 1–3 days before the operation and 10–14 days after the operation by a single investigator (NS) who was unaware of the group assignment during the testing period. The following neuropsychological tests were used for the assessment of cognitive function.

  1. 1. Revised version of Hasegawa’s Dementia Scale (HDS-R): the Hasegawa dementia rating scale (HDS), which is very similar to the Mini-Mental State Examination, is a simple and reliable method and has been widely used in Japan to estimate cognitive impairment (12–15). The HDS-R consists of nine questions to test orientation, immediate and delayed recall of memory, word list generation, and calculation. The scores ranged from 0 to 30 points.
  2. 2. The Benton Revised Visual Retention Test: the Benton Revised Visual Retention Test measures short-term visual memory and visuomotor and visuoconstructional skills, and it requires subjects to draw from memory a series of geometric shapes after a 10-s exposure. This test has a standard criterion for scoring (16–18).

The incidence of cognitive dysfunction can be determined by a change of 1 SD in performance from the preoperative assessment to the postoperative assessment (19–21). In this study, "significant cognitive decline" was defined as present if, in any test, the difference in score for a given test exceeded the preoperative SD for that test. Patients were then divided by use of that criterion into the Normal group or the Decline group.

The variables of the Decline and Normal groups were compared with a Mann-Whitney U-test or by {chi}2 statistical analysis. To compare the differences of cerebral hemodynamic variables between and within the groups, two-way analysis of variance with repeated measures, followed by Fisher’s protected least significant difference test, was used. Furthermore, for determination of the significant predictors of postoperative cognitive impairment, associations with this categorical outcome (normal/decline) were evaluated with logistic regression modeling. Predictor variables measured at eight points were tested both individually (univariate) and together in multivariate forward and backward stepwise selection. After selection of significant predictors (P < 0.05), nonsignificant factors were eliminated and, by use of measure points at which many significant factors were observed (Times 2 and 4), significant factors were tested in multivariate forward stepwise selection. Differences were considered significant at P < 0.05.


   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Significant declines were observed in 15 patients. Patients’ data, including age, sex, surgical procedure, cross-clamp time, CPB time, and transfusion are shown in Table 1. There were no statistical differences between the two groups. The median scores with ranges for each neuropsychological measure of the two groups are shown in Table 2. There were no significant differences in preoperative scores of the HDS-R and the Benton Revised Visual Retention Test between the two groups, nor were there significant differences in postoperative scores. Postoperative scores of the HDS-R and Benton Revised Visual Retention Test were significantly lower in the Decline group than in the Normal group (P < 0.05).


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  		Table 1. Patient Data
 

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  		Table 2. Neuropsychological Variables
 
Changes in physiologic variables in the Normal and Decline groups are shown in Table 3. There were no significant differences in MAP, arterial pH, PaCO2, PaO2, SaO2, rectal and tympanic temperatures, or Hb between the two groups. Figure 1 shows the time course for changes in variables between the Normal and Decline groups. Ca-jvO2 and COER at Times 2 and 4, P50 at Times 2 and 7, and PjvCO2 at Times 2 and 8 were significantly lower in the Decline group than in the Normal group (P < 0.05). PjvO2 and SjvO2 at Times 2 and 4 were significantly higher in the Decline group than in the Normal group (P < 0.05).


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  		Table 3. Physiologic Variables in the Normal (n = 20) and the Decline (n = 15) Groups
 


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  		Figure 1. The changes in arteriojugular venous oxygen content difference (Ca-jvO2), cerebral oxygen extraction ratio (COER), P50, PjvCO2, and SjvO2 between the Normal and Decline groups. Values are expressed as mean ± SD. CPB = cardiopulmonary bypass. #P < 0.05 versus the Normal group with two-way analysis of variance with repeated measures. *P < 0.05 with univariate logistic regression analysis. Each variable was measured at the following time points: 1) just after the induction of anesthesia; 2) 10 min after the beginning of surgery; 3) at 28°C during stable hypothermic CPB; 4) at 30°C during rewarming; 5) at 34°C during rewarming; 6) at the cessation of CPB; 7) 60 min after the cessation of CPB; and 8) at the end of the operation.

 
Of the predictors tested by univariate logistic regression analysis, those significantly associated with impairment are Ca-jvO2 (Times 2 and 4), COER (Times 2 and 4), P50 of jugular bulb venous blood (Time 2), PjvCO2 (Times 2 and 8), PjvO2 (Time 4), and SjVO2 (Times 2 and 4). The ß coefficients, {chi}2 values, and P values from the logistic regression model are shown in Table 4. Table 5 gives the ß coefficients and P values from the logistic regression model, applied to data from time points 2 and 4.


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  		Table 4. Predictors of Postoperative Cognitive Decline
 

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  		Table 5. Predictors of Postoperative Cognitive Decline with Multivariate Regression Analysis
 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
The results of this study show that cognitive function, as assessed by the HDS-R test and the Benton Revised Visual Retention Test, was postoperatively declined in 43% (15 of 35) of patients who underwent cardiac surgery with hypothermic CPB. The incidence of postoperative cognitive decline was significantly associated with high SjVO2 and lower cerebral oxygen extraction. In the Decline group, the P50 value was significantly lower before and after CPB, but not during CPB, than the Normal group, indicating an increased oxygen affinity to Hb before and after CPB.

A number of studies have investigated the etiology of neuropsychological dysfunction after cardiac surgery (1–4). Although its etiology remained unresolved, possible factors reported include age, years of education, MAP, temperature, SjVO2, and emboli. Intraoperative hypotension and cerebral hypoperfusion during CPB have also been cited as potential sources of neurologic dysfunction. Moreover, new instruments, such as the fiberoptic oximetry catheter, facilitate assessment of the adequacy of global cerebral oxygenation. Croughwell et al. (6) demonstrated that inadequate cerebral oxygenation at rewarming during CPB was associated with cognitive dysfunction after cardiac surgery. In contrast, in this study, postoperative cognitive decline was associated with higher SjVO2. The reasons for this contradictory result are unknown. However, various reasons may explain the finding that higher SjVO2 leads to cognitive decline.

First, as Murkin and Buchan (10) point out, increased cerebral blood flow, more than the demand of cerebral oxygen consumption, which may show higher SjVO2, could deliver more emboli into the cerebral circulation. Higher SjVO2 may therefore indicate the effect of the exposure to increased numbers of emboli. Pugsley et al. (22) showed a significant association between the number of emboli and cognitive outcome. Increased cerebral blood flow might transport more emboli and be associated with cognitive decline. Second, lower P50, which indicates the shift of the ODC to the left and increased oxygen affinity to Hb, would cause inadequate tissue oxygenation and higher SjVO2 (9). Coetzee and Swanepoel (23) demonstrated that the ODC was shifted to the left during mild hypothermic CPB. The shift of the ODC to the left might unload inadequate oxygen relative to the oxygen consumption of the tissue. In this study, lower P50 was accompanied with high SjVO2 before CPB, but not during CPB. Hence, during CPB, other mechanisms might be involved. Finally, Edelman and Hoffman (24) demonstrated the arteriovenous shunting in cerebral circulation. McCleary et al. (25) assumed that oxygenated blood was shunted to the venous side of the circulation because of bypassing of the cerebral microcirculation. Nonpulsatile CPB results in cerebral capillary collapse, intravascular sludging, and venodilation (26) and may lead to arteriovenous shunting. Therefore, arteriovenous shunting might induce high SjVO2 associated with inadequate tissue oxygenation, and cognitive decline. However, these premises are speculative. Further study is required to clarify the underlying mechanisms.

In the study presented here, not only during hypothermic CPB, but also before CPB, higher SjVO2 was observed in the Decline group compared with the Normal group. Although SjVO2 values were similar between the Normal and the Decline groups just after the induction of anesthesia (Time 1), the SjVO2 value was higher 10 minutes after the start of the operation in the Decline group than the Normal group (Time 2). This suggests that anesthesia- or surgery-related factors might be associated with higher SjVO2 in the Decline group. Noncardiac surgery and cardiac surgery without CPB also cause cognitive dysfunction (27–29). Therefore, in addition to CPB-related factors, other CPB-unrelated factors would be associated with cognitive decline after surgery. Further study with noncardiac surgical patients without CPB is required to clarify the associated predictors.

We examined only short-term cognitive dysfunction after cardiac surgery in this study. It is unknown whether high SjVO2 could predict long-term cognitive dysfunction after cardiac surgery. Selnes et al. (30) suggested that predictive factors for cognitive decline were different between short-term and long-term studies. In addition, this study is the preliminary study of a small number of patients. Significant association between cognitive decline and higher SjVO2 was observed only at Time 2, although SjVO2 values were higher at Times 2, 3, 4, and 5. To confirm the association between SjVO2 and cognitive dysfunction, further study with more subjects is needed.

In this study, the HDS-R test and the Benton Revised Visual Retention Test were used to evaluate the cognitive function because these tests are often used in Japan. If other tests were used or more tests were combined, the results might be different. However, the incidence of cognitive decline observed in this study was consistent with previous results, and we believe that the influence of the tests used might be small.

In summary, we evaluated the incidence of cognitive decline early after cardiac surgery with hypothermic CPB and assessed whether SjVO2 could be a predictor of postoperative cognitive decline. In 43% of patients, cognitive function declined after surgery. In patients with postoperative cognitive decline, the intraoperative SjVO2 value was higher than in those without cognitive decline. Under conditions in which the oxygen affinity to Hb is increased, SjVO2 might not reflect the tissue oxygenation state. In the future, in addition to SjVO2, monitoring of the tissue oxygenation state will be required to clarify the mechanisms of cognitive decline after cardiac surgery.


   Acknowledgments
 
The authors thank Professor Norio Kurumatani, Department of Hygiene, Nara Medical University, for his assistance in statistical analysis and preparing the manuscript.


   References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication February 7, 2001.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins and Stanford University Libraries' HighWire Press®. Copyright 2001 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press