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Ann Thorac Surg 2008;85:554-560. doi:10.1016/j.athoracsur.2007.09.050
© 2008 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Nursing Neurologic Assessments After Cardiac Operations

Anna T. Bickert, MSN, RNa, Cindy Gallagher, BSN, RNa, Amy Reiner, BSN, RNa, Walter J. Hager, BSN, RNa, Mark M. Stecker, MD, PhDb,*

a Department of Nursing, Geisinger Medical Center, Danville, Pennsylvania
b Department of Neurology, Geisinger Medical Center, Danville, Pennsylvania

Accepted for publication September 26, 2007.

* Address correspondence to Dr Stecker, Department of Neurology, Geisinger Medical Center 100 N Academy Rd, Danville, PA 17822 (Email: mark_stecker{at}yahoo.com).


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Although the neurologic status of patients undergoing cardiac operations has been well studied at other times, there are few studies of neurologic status in the immediate postoperative state. This study used standardized nursing neurologic evaluations to describe the sequence of neurologic changes during the first few hours after cardiac operations and the factors that influence them.

Methods: In this prospective study, patients arriving in the intensive care unit after cardiac operations were serially assessed using the using the Neurologic Intensive Care Evaluation (NICE) for up to 24 hours postoperatively. The study evaluated the effects on outcome of various preoperative and intraoperative variables, as well as the NICE scores.

Results: Recovery of brainstem reflexes occurred at 1.4 ± 1.4 hours, and the fully alert state occurred at a mean of 5.1 ± 3.8 hours after admission to the intensive care unit in patients without a new neurologic deficit. Patients with new neurologic deficits or patients discharged to supervised care settings took longer to reach each neurologic milestone. Older patients, patients with more complex surgical procedures, and patients with higher cardiovascular risk factors took longer to become fully alert. The time to reach the highest NICE score was a strong predictor of the duration of intubation but only weakly predicted other outcome variables in a multivariable analysis.

Conclusions: Standardized, serial nursing neurologic assessments of postoperative cardiac patients provide insight into the immediate postoperative period and may be a useful tool for early identification of patients at risk for adverse outcomes.


    Introduction
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Throughout the course of a cardiac operation, from the preoperative, intraoperative, and immediate postoperative periods to the late postoperative period, there is risk of neurologic injury that may be the source of substantial morbidity and reduction in quality of life [1]. Much research has been dedicated to the study of the preoperative [2] factors that increase the risk for neurologic injury and the effect that the conduct of the operation [3–6] has on the risk of neurologic injury.

There are many studies of the late postoperative neurocognitive outcome [7–9]; however, few studies have been done on the critical immediate postoperative period [10, 11]. Such studies are important because a significant number of neurologic deficits are thought to begin in the postoperative period rather than intraoperatively [7, 23, 24]. Early detection of neurologic injury in the immediate postoperative period may allow for interventions that may ameliorate these deficits. However, formal neuropsychologic testing is impractical in the immediate postoperative period because the patient is intubated and sedated and intensive neurophysiologic monitoring techniques such as electroencephalogram (EEG) [12], evoked potentials [13], and transcranial Doppler [14] imaging that may be used in the operating room are not often used.

The primary goal of this study is to give a detailed picture of the sequence of neurologic changes in the immediate postoperative period using standardized, serial nursing neurologic evaluations with the Neurologic Intensive Care Evaluation (NICE) [11, 15]. Understanding how patients "wake up" after cardiac operations is the first step in early identification of patients at risk for prolonged intubation and a complex neurologic postoperative course. This may lead to early interventions. The second goal was to determine the factors that influenced this sequence of neurologic changes. The third goal was to determine whether neurologic assessments in the immediate postoperative period could predict negative outcomes after cardiac operations.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Patient Sample and Procedures
All research was conducted prospectively in the 19-bed cardiac intensive care unit (ICU) at the Geisinger Medical Center, a 548-bed rural hospital under a protocol approved by the Geisinger Institutional Review Board (#2004-0308), which included a waiver of consent. Any patient admitted to the ICU after a cardiac operation from February 2005 to May 2006 could participate. Patients were excluded if the surgeon requested that the patient not participate, staffing conditions made participation difficult, or if the patient was so medically ill that the nurse would not have the opportunity to obtain the study data. Of 654 candidates, 119 were excluded because of the absence of a rater, 56 because of an intraaortic balloon pump, 36 because they were medically unstable, and 107 for other reasons. Incomplete neurologic assessments resulted in 18 patients being excluded, and 4 were excluded because the primary operation was noncardiac.

On arrival at the ICU, nurses collected the following data:

demographics, including age, weight, and sex;
• information on risk factors, including carotid disease, preoperative stroke, diabetes mellitus, peripheral vascular disease, renal failure, dialysis dependence, acute myocardial infarction, left ventricular dysfunction, sedation sensitivity, hypertension, cancer, and whether the patient was in critical condition before the operation; and
• the surgical procedure, including type of surgical procedure and its duration, number of coronary artery bypass grafts, valves repaired or replaced, duration of cardiopulmonary bypass (CPB), whether circulatory arrest was used, whether any aortic surgery was undertaken, whether the surgery was performed as an emergency.

Information about intraoperative management included lowest intraoperative blood pressure, amount of fresh frozen plasma, platelets, crystalloid, and albumin, the use of Amicar (Wyeth-Ayerst, Collegeville, PA) or aprotinin, as well as the amount of various paralytic and anesthetic agents, and pain medications. The pharmacokinetics of these agents are complex, and so four simple indices were abstracted from the data: total amount of narcotic given during surgery in fentanyl equivalents, total amount of benzodiazepines given during surgery in lorazepam equivalents, total amount of paralytic in vecuronium equivalents, and the maximum end-tidal isoflurane concentration.

The European System for Cardiac Operative Risk Evaluation (EuroSCORE) [18–21], a known predictor of outcome after cardiac operations, was computed.

The NICE was used to assess each patient’s neurologic status in the postoperative period. The NICE scale [11, 15] (Fig 1) is a simple, validated tool developed specifically to assess the postoperative cardiac patient. The values of the NICE scale range from 0 (absent brainstem reflexes) to 8 (alert and oriented) and do not rely on verbal responses. After training, one of 26 nurses (averaging 12 years of critical care experience) performed these neurologic evaluations every 30 minutes from the time of arrival for the first 9 hours and then at 12, 16, and 24 hours after admission to the ICU.


Figure 1
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Fig 1. Illustration of the Neurologic Intensive Care Evaluation (NICE) evaluation. (From Beauchamp K, Baker S, McDaniel C, et al. Reliability of nurses’ neurological assessments in the cardiothoracic surgical intensive care unit. Am J Crit Care, 2001;10:298–305. Reprinted with permission from the American Association of Critical-Care Nurses.)

 
The mean arterial blood pressure was recorded at each assessment point as was the administration of any sedation since the last assessment. Evaluations stopped once the patient first reached the highest level of the NICE scale. No attempt was made to change the standard postoperative care for this observational study.

Pain management typically consisted of hourly doses fentanyl (50 to 100 µg) administered as needed for pain, and ventilator management followed a standardized protocol adopted for all ICU patients. Because pain management and the reversal of paralysis in the ICU setting might alter the process of waking up, three variables were used to explore this possibility: whether any pain medications were given in the first 4 hours in the ICU, whether pain medications were given more than once during that time, and whether any reversal of neuromuscular blockade was given during this time.

Outcome measures included hours intubated, hours in the ICU, days in the hospital postoperatively, the discharge status (home, supervised care, or death), and whether a new intraoperative or postoperative neurologic deficit was manifested by delirium or stroke.

Analysis
Raw NICE scores were transformed into the time when the patient first attained or exceeded a given NICE score. If the patient never reached a given NICE score and neurologic assessments had been made out to 24 hours, the time to reach that score was set to 24 hours. If assessments were not made out to 24 hours, the time to achieve that score was set as missing data.

To determine factors influencing the wake-up time, three measures of wakefulness were studied: return of brainstem reflexes (NICE = 1), return of minimal consciousness (NICE = 4), and recovery to full consciousness (NICE = 8). A Spearman rank correlation was performed between the descriptive variables previously mentioned and the times to reach the three NICE scores. A stepwise multiple linear regression analysis including those explanatory variables (p < 0.05) in the univariable analysis was then used to determine those factors influencing the time to each score. To illustrate the effect of a new neurologic deficit on wake-up times, a repeated measures analysis of variance was used with the times to achieve each NICE score as dependent variables and whether there was a new neurologic deficit as an independent variable. A similar analysis was performed to determine the effect of discharge status on wake-up times. Considering the process of reaching fully oriented state (NICE = 8) as a survival process, a Kaplan-Meier survival analysis was performed in patients with and without a new neurologic deficit. Data from patients that never reached a NICE score of 8 during the assessment period were censored. The log-rank test and the Cox-Mantel test were used to determine statistically significant differences. Data were analyzed using Statistica software (StatSoft, Tulsa, OK).

To understand the factors influencing outcome, multiple analyses were undertaken. The Student t test determined which continuous factors depended on discharge status. Analyses of two-by-two tables were performed to determine which binary factors were significantly different in patients with different discharge status. Spearman rank correlation analyses were used to determine factors associated with outcome variables. Variables with a statistically significant (p < 0.05) correlation coefficient were entered into multivariable analyses. A forward stepwise multiple linear regression analysis was used to find variables independently associated with the continuous outcome variables. A forward stepwise logistic regression calculated with SPSS software (SPSS Inc, Chicago, IL) was used to determine factors independently associated with discharge status.

The above analyses were done both on all patients and in the smaller group undergoing only coronary artery bypass grafting (CABG).


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Of the 315 patients in the study, 179 had only CABG and 135 underwent other procedures, including aortic valve repair/replacement, with or without CABG (Table 1).


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Table 1 Demographics of Patient Population a
 
Basic Observations
After cardiac operations, the average patient (without new neurologic deficit) experienced the return of corneal and pupillary responses (NICE = 1) in 1.4 ± 1.4 hours, with return of responses to painful stimulation (NICE = 2) at 2.6 ± 2.2 hours. The patient begins to follow commands (NICE = 4) 2.9 ± 2.3 hours after arrival in the ICU and becomes fully oriented (NICE = 8) at 5.1 ± 3.8 hours. Figure 2 shows the time required to reach each NICE score as a function of discharge status and postoperative neurologic status. Prolonged times to reach the higher NICE scores in patients with neurologic deficits and patients not discharged to home were significant by analysis of variance (p < 0.001). Figure 3 shows the number of patients that did not reached the fully oriented state (NICE = 8) as a function of time and discharge status. Shorter times to achieve NICE = 8 in patients discharged to home were significant by both the log-rank test (p < 0.00001) and the Cox-Mantel test (p < 0.0003). In patients undergoing only CABG, a significant effect persists by both the log-rank test (p < 0.02) and the Cox-Mantel test (p = 0.05).


Figure 2
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Fig 2. (A) Graph of the time to achieve each Neurologic Intensive Care Evaluation (NICE) score in patients as a function of discharge status to home (filled circles) or elsewhere (open circles). (B) Graph of the time to achieve each NICE score in patients with (open circles) and without (filled circles) new postoperative neurologic deficits. Data are presented with the standard deviation.

 

Figure 3
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Fig 3. Kaplan-Meier survival curves using reaching a Neurologic Intensive Care Evaluation (NICE) score of 8 as criterion in patients as a function of discharge status to home (solid line) or elsewhere (dashed line). The numbers represent the patients at risk in each group.

 
Factors Affecting Wake-Up Times
The surgical procedure had a significant effect on the time to achieve the NICE scores. Patients undergoing cardiac operations other than CABG had prolonged times to achieve each NICE score. The time to achieve NICE = 8 was 4.18 hours in the CABG only group and 6.83 hours in the group undergoing other procedures (p < 0.000001). However, patients undergoing other procedures had higher EuroSCORES than patients undergoing CABG (6.93 vs 4.09, p < 0.000001), suggesting that this group had a greater degree of cardiovascular risk. There is also suggestion that CPB may prolong return to consciousness. In patients undergoing CABG only, the times to achieve NICE scores of 2 to 7 were significantly prolonged in patients undergoing CPB (on-pump) compared with patients who did not have CPB (off-pump) despite similar EuroSCORES and sedation management in each group. The average time to achieve a NICE score of 4 was 2.24 hours in the off-pump group and 4.25 hours (p < 0.0002) in the on-pump group. There was a trend toward prolongation in the time to achieve full orientation (NICE = 8) 4.12 hours in the off-pump group vs 7 hours in the on-pump group (p = 0.055).

Multivariable analysis was used to search for other factors influencing wake-up times in the patients undergoing only CABG. The time for brainstem responses to return (NICE = 1) increased with age (slope, 0.022 h/y; p < 0.0006). The time to reach minimal wakefulness (NICE = 4) increased with the total paralytic dosage (slope, 0.057 h/mg vecuronium equivalent; p < 0.0006), EuroSCORE (0.126 hours, p < 0.02), age (slope, 0.036 h/y; p < 0.004), and previous surgery (slope, 0.74 hours; p < 0.003). The time to achieve NICE = 8 was also prolonged in older patients (slope, 0.062 h/y; p < 0.007) and patients with a higher EuroSCORE (slope, 0.25 hours; p < 0.008). The administration of pain medications in the postoperative state had slight effects on the wake-up times, because only 3.5% of patients received any pain medications in the first 4 hours in intensive care.

Predicting Outcomes
Table 1 summarizes the values of selected relevant preoperative and intraoperative factors in patients that were discharged to home and patients that were not. The Appendix summarizes the univariable relationships between the explanatory variables and the outcome measures. Men, older patients, diabetes patients, and patients with chronic renal failure were less likely to be discharged to home. Patients undergoing aortic valve repair/replacement, on-pump procedures, or any procedure other than CABG were also less likely to be discharged to home.


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Appendix Univariable Effects on Outcome Measures (Spearman R) in the Complete Group of Patients
 
The total amount of paralytic and narcotic agents given during surgery did not affect outcome, although patients receiving higher doses of benzodiazepines were slightly less likely to return home.

Patients with higher EuroSCORES and patients with prolonged times to reach various NICE scores were also less likely to be discharged home. The probability of discharge other than to home was 6.4 times more likely in patients taking more than 8 hours to reach NICE 8 (p < 0.003). In addition, the duration of intubation was five times longer (53 hours vs 11 hours, p < 0.0001), the duration of time in intensive care was twice as long (146 vs 67 hours, p < 0.0001), and the length of the hospital stay was almost twice as long (11 vs 6.42 days, p < 0.0001) in patients who took more than 8 hours to reach the state of NICE = 8. In patients undergoing only CABG, the duration of intubation was the only outcome measure that was different in those who took more or less than 8 hours to reach NICE = 8.

Because there are a number of explanatory variables, a multivariable analysis is important in determining which variables have independent predictive power. It is especially useful to consider patients that underwent only CABG because of the previously demonstrated effects of surgery type. The factors influencing the duration of intubation are EuroSCORE (slope, 0.52 hours; p < 0.001), time to NICE = 8 (slope, 0.82; p < 0.000001), and cancer (slope, 5.03; p < 0.00002). The average time between achieving a NICE score of 8 and extubation was 11.2 hours. The factors predicting the time in the intensive care unit were preoperative stroke (slope, 43.6 hours; p < 0.00002), diabetes (slope, 19.7 hours; p < 0.002), and cancer (slope, 25.0 hours; p < 0.003). The factors predicting number of days in the hospital were diabetes (slope, 1.60 days; p < 0.0005) and EuroSCORE (slope, 0.22 days; p = 0.005). The logistic regression analysis used to predict discharge status yielded complex results suggesting that increasing age, male sex, and increased intraoperative transfusion requirements were predictors of poor discharge status.


    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
This study used a standardized evaluation tool, the NICE, to quantify the neurologic events occurring in the period immediately after cardiac operations. It demonstrated an orderly progression that, in patients who do not sustain a new neurologic injury, is characterized by recovery of brainstem reflexes at 1.4 ± 1.4 hours, the minimally conscious state at an average of 2.9 ± 2.3 hours, and the fully oriented state at 5.1 ± 3.8 hours.

This sequence of neurologic events was influenced by many factors. In univariable analyses, patients with a new neurologic deficit or patients who were not discharged to home took significantly longer to reach each NICE score. This prolongation was greater for larger NICE scores because larger NICE scores depend on higher integrative functions of the brain that are more sensitive to any type of injury, a phenomenon that has been demonstrated in studies of neurologic status after cardiac arrest [17] and head injury [16]. The time to reach each NICE score was significantly influenced by the surgical procedure. Patients undergoing procedures other than CABG and patients who underwent on-pump CABG had longer times to wake up than patients who underwent off-pump CABG.

Many variables could influence an outcome as complex as recovery of consciousness so a multivariable analysis was performed. This analysis suggested that these effects may be primarily related to patient age and to the degree of cardiovascular risk as quantified by the EuroSCORE. It also indicated that the amount of anesthetic agents and narcotic drugs given during surgery and the amount of sedation administered in the intensive care unit had little effect on the wake-up times.

The third goal of this study was to elucidate factors influencing patient outcomes. In univariable analyses, patients who took longer than 8 hours to reach NICE = 8 had significantly poorer outcomes, and prolonged intubation and ICU and hospital lengths of stay. In the multivariable analysis, larger EuroSCORE, increased time to achieve NICE = 8, and cancer were associated with prolonged duration of intubation. The duration of time in the ICU was increased in patients with diabetes, cancer, and preoperative stroke. The length of hospital stay was prolonged in patients with diabetes and a larger EuroSCORE. Discharge status was influenced by a combination of age, sex, and intraoperative transfusion management.

That the time to achieve the fully alert and oriented state (NICE = 8) is strongly predictive of the time of intubation in both univariable and multivariable analyses indicates that formal nursing neurologic assessments may be helpful in developing and implementing an early extubation program, which has been suggested [22] as the nursing intervention most likely to improve outcomes of cardiac operations.

There are problems with multivariable analyses. When strong correlations exist between many explanatory variables, such as age, EuroSCORE, surgical procedure, neurologic injury, and the time to achieve each NICE score, selecting the variables most likely to contribute to a given result can be difficult. Thus, a factor that does not appear significant in the multivariable analyses but is significant in the univariable analysis may still have importance in predicting the dependent variable. So although the time to achieve a NICE score of 8 did not enter into the multivariable predictive models of time in intensive care, duration of hospital stay, or discharge status, prolonged times to achieve a NICE score of 8 may still provide a signal to nurses and physicians that there is a potential problem that should be investigated. The value of this indicator will await future trials of nursing interventions based on neurologic assessments.

This study has some limitations. Although it was a prospective study, the study sample excluded the sickest patients. This reduces the prevalence of neurologic injury in the study sample and hence the chance that a neurologic assessments would be helpful. This is reflected in the stronger dependences on time to reach NICE = 8 in the complete group of patients than in the group of patients undergoing only CABG. This suggests that if the NICE were applied to all patients having cardiac operations, a greater effect would be noted.

Second, this study was done at a single hospital with a single approach to cardiac operations, and so the data obtained may not be valid for other institutions with different protocols. In a pilot study [11] at a different hospital, however, the average time to achieve minimal consciousness (NICE = 4) was 2.88 hours compared with 2.9 hours in this study, and the time to achieve full orientation (NICE = 8) was 4.9 hours compared with 5.1 hours in the current study. Thus, it may be that slight variations in nursing protocols from one institution to another may not have large effects on the wake-up times.

Finally, no account for the actual pharmacokinetics of the medications administered was made. Clearly, this will be a factor in determining wake-up times and future investigations may take this into account.


    Appendix
 


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
We wish to thank Jen Costello, NA, for her great help in data entry and management. In addition, we wish to thank Dr Charles Benoit, Dr Edward Woods, and Dr Serrie Lico for their cooperation.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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