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CARDIOVASCULAR ANESTHESIA

Slow Rewarming Has No Effects on the Decrease in Jugular Venous Oxygen Hemoglobin Saturation and Long-Term Cognitive Outcome in Diabetic Patients

Yuji Kadoi, MD^*, Shigeru Saito, MD^*, Fumio Goto, MD^*, and Nao Fujita, MD

*Department of Anesthesiology and Reanimatology, Gunma University, School of Medicine; and Department of Anesthesiology, Keiyu Orthopedic Hospital, Gunma, Japan

Address correspondence and reprint requests to Yuji Kadoi, MD, Department of Anesthesiology and Reanimatology, Gunma University, School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 371-8511, Japan. Address e-mail to kadoi{at}med.gunma-u.ac.jp

	Abstract

Top Abstract Introduction Patients and Methods Results Discussion References

 
The purpose of this study was to examine the effects of rewarming rate on internal jugular venous oxygen hemoglobin saturation (SjvO₂) during the rewarming period, and long-term cognitive outcome in diabetic patients. We studied 30 diabetic patients scheduled for elective coronary artery bypass graft surgery. As a control, 30 age-matched nondiabetic patients were identified. The diabetic patients were randomly divided into two groups: the Slow Rewarming group (n = 15) (mean rewarming speed: 0.22° ± 0.07°C/min, mean ± SD) or the Standard Rewarming group (Standard group) (n = 15) (mean rewarming speed: 0.46° ± 0.09°C/min, mean ± SD). After the induction of anesthesia, a fiberoptic oximetry catheter was inserted into the right jugular bulb to monitor SjvO₂ continuously. Hemodynamic variables and arterial and jugular venous blood gases were measured at nine time points. All patients underwent a battery of neurologic and neuropsychologic tests on the day before the operation and at 4 mo after surgery. The SjvO₂ values in the Standard group were decreased during the rewarming period compared with at the induction of anesthesia (P < 0.05). There was a significant difference in the SjvO₂ value in the Control group between standard rewarming and slow rewarming during rewarming periods (Standard Control group: 51% ± 8%, Slow Control groups: 58% ± 5%) (P < 0.05). However, there was no difference in the SjvO₂ value in diabetic patients between standard rewarming and slow rewarming during the rewarming period. The rewarming rates (odds ratio: 0.8; 95% confidence interval: 0.5–1.3; P = 0.6) had no correlation with cognitive impairment at 4 mo after the surgery. Diabetes (odds ratio: 1.6; 95% confidence interval: 0.9–2.6; P = 0.04) was a factor in relation to cognitive impairment at 4 mo after the surgery. We concluded that a slow rewarming rate had no effects on the reduction in SjvO₂ value and long-term cognitive outcome in diabetic patients.

IMPLICATIONS: We examined the effects of rewarming rate on internal jugular venous oxygen hemoglobin saturation in diabetic and nondiabetic patients during the rewarming period and long-term cognitive outcome. Slow rewarming could not prevent the frequency of the reduction in internal jugular venous oxygen hemoglobin saturation and adverse cognitive outcome in diabetic patients.

	Introduction

Top Abstract Introduction Patients and Methods Results Discussion References

 
Preexisting diabetes mellitus is one of the major factors related to an adverse postoperative neurologic outcome after cardiac surgery (1). The mechanisms of postoperative cognitive dysfunction in diabetic patients after cardiac surgery, however, are not fully understood (1).

Croughwell et al. (2) reported that patients with diabetes mellitus had abnormal cerebral autoregulation during hypothermic cardiopulmonary bypass (CPB). They found that the cerebral desaturation state, estimated by jugular venous oxygen hemoglobin saturation (SjvO₂) <50%, was more often observed in diabetic patients than in nondiabetic patients during the rewarming period at hypothermic CPB. Previously, we found that diabetic patients more often experienced cerebral desaturation than nondiabetic patients during normothermic CPB (3). Additionally, moderate hypothermia (32°C) could prevent a cerebral desaturation state in diabetic patients (4).

There have been some reports showing that both nondiabetic patients and animals who were warmed rapidly had larger reductions in SjvO₂ than those who were warmed slowly (5–7). Grigore et al. (8) reported that slower rewarming rates were better than standard rewarming techniques for improving neurocognitive outcome in nondiabetic patients. We hypothesized that slower rewarming rates were better for improving the SjvO₂ values in diabetic patients. There has been no comparative study regarding the effects of slow rewarming rate and fast rewarming rate on SjvO₂ in diabetic patients. The purpose of this study was to examine the effects of rewarming rate on SjvO₂ during the rewarming period and long-term cognitive outcome in diabetic patients.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Discussion References

 
This study had the approval of the ethics committee of our institution, and written, informed consent was obtained from all patients. Thirty diabetic patients scheduled for elective coronary artery bypass graft surgery were studied. Table 1 shows the specific data of the diabetic groups. The types and amounts of antidiabetic drugs, preoperative fasting blood glucose, and complications were almost similar between the diabetic groups.

Patients were randomly assigned to two groups: the Slow Rewarming group (n = 15) or the Standard Rewarming group (n = 15). As a control, 30 age-matched nondiabetic patients consecutively scheduled for elective coronary artery bypass graft surgery were also randomized to standard versus slow rewarming.

All patients received 10 mg of diazepam per os 1 h before anesthesia. Anesthesia was induced with 0.2 mg/kg midazolam, 10 µg/kg fentanyl, and 0.2 mg/kg vecuronium. The trachea was intubated. After the induction of anesthesia, a pulmonary arterial catheter (Vigilance^® Swan-Ganz CCO Thermodilution Catheter; Baxter, Irvine, CA) was inserted through the right internal jugular vein. For continuous monitoring of SjvO₂, a 4.0F fiberoptic oximetry oxygen saturation catheter (Dual-Lumen Oximetry Catheter^®; Baxter) was inserted into the right jugular bulb by using a modified Seldinger technique. This catheter was connected to an analysis system (Explorer^TM System; Baxter) and calibrated in vivo by drawing a blood sample from the catheter. The position of the jugular bulb catheter was verified by radiograph. The SjvO₂ readings were collected and processed in a monitor-computer interface, and displayed and stored every 5 s in an Apple Macintosh computer (Apple Macintosh Computer Co., Ltd., Cupertino, CA).

The partial pressures of the arterial and jugular venous blood gases were analyzed by using a Stat Profile Ultmita^® (NOVA Biomedical Co., Boston, MA) and CO-oximeter (OSM3 Hemoximeter^®; Radiometer Co., Copenhagen, Denmark). All patients’ lungs were ventilated with oxygen 50% and N₂ 50%. PETCO₂ was monitored (Ultima^®; Datex, Helsinki, Finland) and maintained between 35–40 mm Hg. Anesthesia was maintained with a large dose of fentanyl (total dosage of fentanyl:76.4 ± 13.9 µg/kg, mean ± SD). Muscular relaxation was achieved by intermittent administration of vecuronium. No volatile anesthetic was administered. The tympanic temperature was continuously monitored by using Mon-a-Therm^® (Mallinckrodt Co., St. Louis, MO).

During rewarming, a 1°–2°C difference between tympanic temperature and CPB perfusate temperature was maintained for patients enrolled in the Slow group and a 4°–5°C difference for patients enrolled in the Standard group. PaO₂ was maintained at 150 to 300 mm Hg during the study.

The CPB was primed with a crystalloid, nonglucose-containing solution, 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, and PaCO₂ uncorrected for temperature was adjusted to normocapnic levels (35–40 mm Hg) by varying fresh gas flow to the membrane oxygenator (-stat regulation). The target tympanic temperatures was 30°C.

Hematocrit was maintained at >0.20 on CPB, with the transfusion of blood if necessary. Phenylephrine infusions were used during CPB to maintain a mean arterial blood pressure (MAP) of 50–90 mm Hg. Distal coronary anastomoses and proximal anastomoses were performed during a single aortic cross-clamp. Hemodynamic variables and arterial and jugular venous blood gases were measured at different time points: 1 = after the induction of anesthesia and before the start of surgery, 2 = at the onset of CPB, 3 = just after cooling to 30°C, 4 = during stable hypothermia at 30°C, 5 = at the end of stable hypothermia, 6 = at 33°C during rewarming, 7 = just after the rewarming to 36°C, 8 = at the cessation of CPB, and 9 = at the end of the operation. Intraoperative epiaortic ultrasonography confirmed that none of the patients had moderate or severe atherosclerotic lesions in the ascending aorta.

All patients underwent a battery of neurologic and neuropsychologic tests on the day before the operation and at 4 mo after surgery, administered by trained specialists with intra- and interobserver validity ensured. The examiners who administered the cognitive tests were unaware of the patient’s intraoperative treatment assignment. The neuropsychologic portion of the study design followed the consensus statements on the assessment of central nervous system disorders after cardiac surgery (9).

Cognitive functioning was assessed by using the following tests: 1) mini-mental state examination, 2) Rey auditory verbal learning test, 3) trail-making test (part A), 4) trail-making test (part B), 5) digit span forward, and 6) grooved pegboard.

All data were expressed as means ± SD. After confirming equal variance among the groups by the Bartlett test, changes in the mean values such as hemodynamic variables and SjvO₂ were compared with the baseline values by using an analysis of covariance. Variables at Period 1 were used as a covariant. Contrast was used to compare the differences among the four groups at each time point. For multiple comparison, the Bonferroni method was used. To eliminate a type II error, each individual P value was adjusted.

After the study was completed, we evaluated the sample size. The sample size calculation was based on the hypothesis that the SjvO₂ value in diabetic patients would be decreased by 10% compared with that in control patients. The sample size provides 70% power to detect a 30% difference between groups with a 5% probability of an a-type error.

The difference between the preoperative values and those at 4 mo after the operation on neuropsychologic tests was assessed with the paired t-test method. To obtain an indicator of outcome overall, significant impairment was defined as a decline from preoperative testing of >1 SD on >20% of test measures (at least 2 of 6). A multivariable logistic regression with odds ratio was used to examine the predictive variables of adverse outcome at 4 mo.

Statistical significance was set at P < 0.05. All calculations were performed on a Macintosh computer with SPSS (SPSS Inc., Chicago, IL) and StatView 5.0 software packages (Abacus Concepts Inc., Berkeley, CA).

	Results

Top Abstract Introduction Patients and Methods Results Discussion References

 
There were no significant demographic differences among the four groups (Table 2). MAP was decreased during the CPB period in the four groups compared with that in Period 1 (Table 3). There were no differences in MAP, cardiac index, or PaCO₂ among the four groups during the study at a given timepoint.

View larger version (17K): [in this window] [in a new window]   Figure 1. A and B, The time course of changes in SjvO2 values in the Diabetic and Nondiabetic groups in the Fast or Slow Rewarming groups. Values are means ± SD; *P < 0.05 compared with period 1, #P < 0.05 compared with the Slow group, $P < 0.05 compared with the Control group. 1 = After the induction of anesthesia and before the start of surgery, 2 = at the onset of CPB, 3 = just after cooling to 30°C, 4 = during stable hypothermia at 30°C, 5 = at the end of stable hypothermia, 6 = at 33°C during rewarming, 7 = just after rewarming to 36°C, 8 = at the cessation of CPB, and 9 = at the end of the operation.

	Discussion

Top Abstract Introduction Patients and Methods Results Discussion References

There have been controversial reports regarding the effect of the rewarming rate on the SjvO₂ value in nondiabetic patients (5–7,10). Nakajima et al. (6) reported that the percent decrease in SjvO₂ was significantly related to rewarming speed in nondiabetic patients. In contrast, von Knobelsdorff et al. (10) found that prolonged rewarming after hypothermic CPB did not attenuate the reduction in SjvO₂. Our result is inconsistent with that of von Knobelsdorff et al. This discrepancy might be in part attributable to the difference in demographic data of patients or anesthetic drugs. von Knobelsdorff et al. did not differentiate between patients with diabetes shown to have abnormal autoregulation during rewarming (2). Moreover, von Knobelsdorff et al. used a continuous infusion of etomidate during the rewarming period. Etomidate can cause cerebral vasoconstriction (8). Our findings confirmed that a slow rewarming rate could attenuate the reduction in SjvO₂ during rewarming in nondiabetic patients.

There have been few reports describing the changes in SjvO₂ during CPB in diabetic patients (2–4). In previous studies (3,4), we found that SjvO₂ in diabetic patients during normothermic CPB was reduced compared with that in controls, and that no reduced SjvO₂ in diabetic patients was observed during hypothermic CPB. However, we did not examine any effect of the SjvO₂ on postoperative cognitive dysfunction. Moreover, we did not assess the detailed changes in SjvO₂ during the rewarming period when reduced SjvO₂ was often observed. In this study, we found a reduced SjvO₂ during the rewarming period in diabetic patients. Croughwell et al. (2) found greater desaturation during rewarming in diabetic than nondiabetic patients, and reported that the periods of desaturation were associated with increased oxygen extraction and loss of the normal coupling between cerebral blood flow and cerebral metabolic rate for oxygen. The present findings are consistent with those of Croughwell et al. Our findings confirm that the rewarming period is a risk period when reduced SjvO₂ is often observed in diabetic patients.

Newman et al. (11) reported that rewarming speed had no independent effect on postoperative cognitive decline in nondiabetic patients. However, in a recent study, Grigore et al. (8) reported that slower rewarming rates were better than standard rewarming techniques for improving neurocognitive outcome in nondiabetic patients. There have been no reports regarding the effect of the rewarming rate on postoperative cognitive dysfunction in diabetic patients. This is the first study to examine the effect of the rewarming rate on postoperative cognitive decline in diabetic patients. The present data show that reduced SjvO₂ during the rewarming period is not related to long-term postoperative cognitive dysfunction in diabetic patients.

In nondiabetic patients, we could not find any effect of rewarming rates on postoperative cognitive dysfunction. This result observed in the Control group is inconsistent with the data from Grigore et al. (8). This discrepancy might be in part attributable to the difference in anesthetic regime, patient demographic data, the performance test of cognitive dysfunction, or the difference of day when patients were assessed (11,12). In addition, this study has relatively few patients. Although our data show that the rewarming rates had no effects on long-term cognitive outcome, further prospective, randomized trials are necessary to clarify whether the rewarming rate has beneficial effects on postoperative cognitive outcome in diabetic patients.

Enomoto et al. (7) reported, in rabbit models, that reduced SjvO₂ with rapid rewarming was caused by an increase in cerebral metabolic rate for oxygen, which was unmatched by an increase in cerebral blood flow. They suggested that this mismatch might indicate a transient abnormality in the flow-metabolism coupling, or the effect of temperature gradients on oxygen transfer from hemoglobin to the brain. Hindman (13) and Shaaban et al. (14) suggested that patients who desaturated most during rewarming were affected by abnormalities in the flow-metabolism coupling that were present before rewarming. Their suggestions were supported by Goto et al. (15), who observed that there was more SjvO₂ desaturation during rewarming in patients with preoperative evidence of small cerebral infarction. Because diabetic patients might have an abnormality in the flow-metabolism coupling that could not be detected by a preopera-tive examination in this study, we observed the reduced SjvO₂ during the rewarming period in diabetic patients.

Cook et al. (16) demonstrated that cerebral hyperthermia occurred regularly during rewarming from hypothermic CPB. Because it is well known that a difference in the temperature between the CPB circuit and the brain is often observed during rewarm-ing, cerebral hyperthermia might be responsible for the low SjvO₂. In this study, we monitored tympanic temperature continuously. Tympanic temperature is thought to be reflected as brain temperature. Therefore, we do not think that cerebral hyperthermia occurred during rewarming from hypothermic CPB in this study.

Because of the limited time available for neuropsychologic testing preoperatively, we could not cover all major cognitive domains. Further studies are needed to determine whether any correlation exists between SjvO₂ reduction and all major cognitive domains.

It remains controversial whether SjvO₂ during the rewarming period is associated with postoperative cognitive dysfunction (11–14,17). Croughwell et al. (18) reported that lower normothermic SjvO₂ values (at the end of rewarming) were associated with acute cognitive deficits (4–8 days after surgery). Subsequent work by Newman et al. (11), which included most of the patients reported in the study by Croughwell et al., found that SjvO₂ had an extremely small independent association with cognitive impairment 7–10 days after surgery in hypothermic CPB, when baseline cognitive status, age, and years of education were considered in the analysis. Finally, Robson et al. (17) found averaged SjvO₂ values during hypothermic bypass, and in the early postoperative phase, had no association with cognitive status three months after surgery in normothermic CPB. In contrast, Yoshitani et al. (19) reported that high SjvO₂ was associated with cognitive dysfunction after the operation. Further prospective, randomized studies are necessary to identify the association between low or high SjvO₂ value during the rewarming period and cognitive dysfunction.

Robson et al. (17) provided evidence that jugular bulb catheter readings were not very accurate during CPB, possibly because of increased vessel wall contact. However, in previous studies (20,21), we assessed the accuracy of our oximetric catheter system and found an excellent correlation (r² = 0.979) between oximetry catheter values for SjvO₂ and simultaneous SjvO₂ values obtained from samples of jugular venous blood measured in a CO-oximeter.

In this study, we selected a dichotomous outcome analysis. There have been some controversies over which analysis would be more clinically meaningful, a dichotomous outcome or continuous outcome measures (22–24). Grigore et al. (8) reported that the analysis of neurocognitive performance as a continuous measure was more sensitive. Blumenthal et al. (24) reported that, although the arbitrariness of categoric boundaries was avoided in continuous outcome mea-sures, it was difficult to ascertain with this type of analysis the clinical significance of changes. There is no solid agreement whether linear regression is better than logistic regression analysis as a statistical method for assessing the relationship between the risk factors and cognitive dysfunction.

There were slight differences in the SjvO₂ values between the present and previous studies in diabetic patients (3). These differences might be in part attributable to the differences in anesthetic regime, management of CPB temperature, and age (12). Nandate et al. (25) found differential effects of anesthetics on SjvO₂. Moreover, we found that a temperature difference had a great effect on the SjvO₂ value during the CPB period (20).

In conclusion, slow rewarming did not attenuate the decrease in the SjvO₂ value during rewarming and had no effects on the long-term cognitive outcome in diabetic patients.

	Acknowledgments

 
This study was supported in part by a grant (to YK) from the Japanese Ministry of Science and Education.

The authors thank Dr. Martin Mueller (Department of Anesthesiology, University of Texas Medical Branch at Galveston) for his English editing.

	References

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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