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Ann Thorac Surg 1996;61:1295-1296
© 1996 The Society of Thoracic Surgeons
Departments of Anesthesia and Cardiothoracic Surgery, Bowman Gray School of Medicine of Wake Forest University, Winston-Salem, North Carolina
The present debate over the best means of analyzing subtle brain dysfunction as a measure of surgical success is a tribute to the advances in cardiopulmonary bypass and cardiac surgery in the past two decades. However, in the coming years, as the results of cardiac surgery come under increasing scrutiny, further vigilance will be necessary to ensure better outcomes.
Major neurologic dysfunction and death have become rare outcomes after cardiopulmonary bypass-rare enough that they provide insufficient statistical power to be useful as timely measures of whether an intervention is of benefit unless a very large, prohibitively expensive, multicenter trial is undertaken. Furthermore, in today's cyberspace environment, patients expect not only to survive their operation but to be at least as functional as they were before their intervention. To fulfill this expectation, new definitions of what exactly constitutes a positive outcome are required.
What Are Neurobehavioral Tests?
Psychological tests are not just IQ tests or questionnaires about your childhood. They are also short, easy to administer, objective, and sensitive means of assessing the alterations in brain function associated with cardiopulmonary bypass [1]. They provide an attractive, practical alternative to morbidity and mortality statistics. A reliable ``brain function test'' allows the evaluation of surgical and pharmacologic interventions with relatively small numbers of patients. Tests of fine motor function, verbal and nonverbal memory, attention, and concentration are collectively referred to as ``neuropsychological tests'' and are designed as tools to assess the most complex structure on earth, the human brain. ``Neurobehavioral'' is a more inclusive term that includes aspects of neurologic and neuroophthalmologic assessment.
One example of the utility of neuropsychological tests is their routine serial administration to National Football League quarterbacks to assess the cumulative effects of concussion. They are the determining factor in deciding whether a player should retire or play in a given game. The National Football League faces the same dilemma we are discussing here: what constitutes a significant change in brain function? Interestingly, the changes in function required to retire a player are much smaller than the ones discussed in the excellent article published in this issue by Mahanna and co-workers [2].
What Is a Neurobehavioral Deficit?
The definition of neurobehavioral dysfunction depends on the question. Typically a clinical question turns on the issues of severity and clinical significance. Historically, the clinical question has been posed in either of two ways: Has a brain injury caused the patient to be impaired relative to a standard control group, or is there a need to identify a specific deficit that locates the affected brain region and pinpoints the cause? These concerns are not necessarily pertinent to whether cardiopulmonary bypass causes brain injury and whether the trauma is preventable or treatable. Just as with the status of the National Football League player, the surgical team's interest is the relative change in the patient's cognitive abilities from before operation to after operation. The relevant question is not whether these patients have received sufficient injury to be impaired relative to the general population, but whether there is a detectable change in their own cognitive function that could have been prevented.
Another question that is frequently asked is whether the changes in cognitive function after cardiopulmonary bypass are important enough to warrant study. There are problems with hierarchically assigning ``significance'' to a brain function. With a muscle such as the heart or an organ like the liver, the more tissue disrupted the more apparent dysfunction the patient exhibits and the more a test of cardiac or liver function will be abnormal. This not the case with the brain. The location of the lesion is far more critical than the amount of tissue damaged. Hecaen [3] determined that a right hemisphere lesion must be three times larger than a left (dominant) hemisphere lesion, in the homologous anatomic location, before it is noticed by lay people.
Hence, the ``severity'' of a deficit is a subjective opinion and more related to anatomic site than to size or cause of the lesion. It is difficult to rank brain disorders, such as suggesting that an inability to recognize faces is less of a problem than being unable to recognize numbers. Most would agree that hemiparesis is a major catastrophe, but the amount of tissue associated with an internal capsule lesion is minuscule compared with a frontal lobe stroke, where the behavioral dysfunction of perseveration and word finding problems may go unnoticed. For the clinical team, it may not be critical to know where a lesion occurs unless this helps in developing a strategy to prevent trauma to other patients.
As an example of how surgical technique affects outcome, if we increase perfusion to the brain during cardiopulmonary bypass via changes in blood pH or temperature, we may deliver more emboli to the brain and affect the final distribution of the emboli. If the cortex is more metabolically active during an embolic shower, the lesions will be larger; but equally important, the lesions will be in areas where behavioral manifestation of the injury will be more apparent. Instead of being merely slower and clumsier, as in the case of subcortical white matter lesions, the patients are more likely to have specific disorders, such as word finding problems, that are associated with cortical lesions.
What Assessment Tools Should Be Used?
The questions asked by cardiac surgeons, anesthesiologists, and perfusionists deal with (1) assessing the frequency of occurrence of brain injury, (2) determining the cause of the injury and whether the injury is preventable, and (3) if the injury is not preventable, whether there are means to reduce the amount of focal trauma and ameliorate the clinical manifestation of the injury.
To answer these questions a measure of brain function is required that is brief, cheap, and above all, reliable and repeatable. Radiologic measures, transcranial Doppler echography and electroencephalography are not measures of behavior. Neurobehavioral tests do fill the bill, but certain parameters must be accepted by the research community if the information derived is to be useful. These are the same parameters for any assessment tool-they must be used in a consistent manner. Data on hematocrit would not be useful if every institution used different assessment and analysis methods.
No one test will suffice because the brain is a complicated and diverse organ. Second, it is not important which particular tests are used as long as the same tests or types of tests are used and applied in the same manner [4]. Third, the results must be analyzed in the same way across studies so that appropriate comparisons can be made. In our experience, a 20% decline in postoperative neuropsychological function is a significant change and provides a standard by which we can compare results between patient populations separated by time and space [5].
In this issue Mahanna and co-workers [2] have provided an excellent review of the different ways neuropsychological data have been analyzed over the past decade. Using their own data, they have described the advantages and disadvantages of each analysis technique and made useful recommendations about the preferred method.
In the past, these issues were less important because relatively few researchers used neuropsychological tests and it was not yet apparent that results could be used to identify etiologic factors affecting neurobehavioral sequelae after cardiopulmonary bypass. However, several recent studies have demonstrated the utility of these tests in assessing the impact of emboli [5–7], systemic rewarming [8], and surgical technique [9] on the brain. We found a relationship between the number of cerebral emboli detected and the likelihood of postoperative neuropsychological deficits. Changes in venting techniques resulted in a decline in the number of emboli and incidence of neuropsychological deficits [9].
The article by Mahanna and co-workers [2] will be of interest to the growing number of investigators using neurobehavioral testing. Evidence of current interest in protecting the brain during cardiopulmonary bypass is that special editions of both The Annals of Thoracic Surgery [10] and the Journal of Cardiothoracic and Vascular Anesthesia [11] have been devoted recently to the subject.
The appropriate use of neurobehavioral assessment, when combined with technological advances in emboli detection, magnetic resonance imaging, and spectroscopy, can help identify and eliminate various contributing factors that are responsible for brain injury during cardiopulmonary bypass. New surgical techniques, changes in temperature and perfusion strategies, and the efficacy of new neuroprotective agents can be assessed by neuropsychological testing. Thus, the sensitive assessment of neurobehavioral function provides a standardized measure of outcome that serves to improve clinical methods in an age of quality improvement.
Footnotes
Address reprint requests to Dr Stump, Department of Anesthesia, Bowman Gray School of Medicine, Wake Forest University, Medical Center Blvd, Winston-Salem, NC 27157-1009.
References
Related Article
This article has been cited by other articles:
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  G. B. Mackensen, L. K. Ti, B. G. Phillips-Bute, J. P. Mathew, M. F. Newman, H. P. Grocott, and the Neurologic Outcome Research Group Cerebral embolization during cardiac surgery: impact of aortic atheroma burden Br. J. Anaesth., November 1, 2003; 91(5): 656 - 661. [Abstract] [Full Text] [PDF]
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 M. A. Borger and V. Rao Temperature Management During Cardiopulmonary Bypass: Effect of Rewarming Rate on Cognitive Dysfunction Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 2002; 6(1): 17 - 20. [Abstract] [PDF]
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 D. A. Stump, R. L. James, and J. M. Murkin Is that outcome different or not? The effect of experimental design and statistics on neurobehavioral outcome studies Ann. Thorac. Surg., November 1, 2000; 70(5): 1782 - 1785. [Full Text] [PDF]
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J. M. Murkin and D. A. Stump Res ipsa loquitur: protecting the brain in the new millennium, ""outcomes 2000"" Ann. Thorac. Surg., May 1, 2000; 69(5): 1317 - 1318. [Full Text] [PDF]
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K. P. Grichnik, A. J.J. Ijsselmuiden, T. A. D’Amico, D. H. Harpole Jr, W. D. White, J. A. Blumenthal, and M. F. Newman Cognitive decline after major noncardiac operations: a preliminary prospective study Ann. Thorac. Surg., November 1, 1999; 68(5): 1786 - 1791. [Abstract] [Full Text] [PDF]
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D. A. Stump, W. R. Brown, D. M. Moody, K. D. Rorie, J. C. Manuel, N. D. Kon, J. B. Butterworth, and J. W. Hammon Microemboli and Neurologic Dysfunction After Cardiovascular Surgery Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 1999; 3(1): 47 - 54. [Abstract] [PDF]
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J. W. Hammon Jr, D. A. Stump, N. D. Kon, A. R. Cordell, A. S. Hudspeth, T. E. Oaks, R. F. Brooker, A. T. Rogers, R. Hilbawi, L. H. Coker, et al. Risk Factors and Solutions for the Development of Neurobehavioral Changes After Coronary Artery Bypass Grafting Ann. Thorac. Surg., June 1, 1997; 63(6): 1613 - 1617. [Abstract] [Full Text]
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