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Interact CardioVasc Thorac Surg 2005;4:216-221. doi:10.1510/icvts.2004.092528
© 2005 European Association of Cardio-Thoracic Surgery
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ESCVS article - Cardiopulmonary bypass

Cognitive decline after cardiac surgery: proposal for easy measurement with a new test{star}

Yolanda Carrascal*, Elena Casquero, Javier Gualis, Salvatore Di Stefano, Santiago Flórez, Enrique Fulquet, Jose Ramon Echevarría and Luis Fiz

Department of Cardiac Surgery, University Hospital of Valladolid, Valladolid, Spain

Received 12 June 2004; received in revised form 10 November 2004; accepted 10 February 2005

{star} Presented at the 53rd International Congress of the European Society for Cardiovascular Surgery, Ljubljana, Slovenia, June 2–5, 2004.

*Corresponding author: Yolanda Carrascal Servicio de Cirugía Cardiaca. Hospital Universitario de Valladolid Avda. Ramon y Cajal, 3 47005 Valladolid Spain. Tel.: +34 983 420 000.

E-mail address: aguerrerop{at}medynet.com (Y. Carrascal).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Objective: Neuropsychological dysfunction is a recognized complication after cardiac surgery. Attention, concentration, short term memory, and speed of mental processing are commonly involved. We evaluated prospectively the incidence of cognitive impairment in our population using a single test: Paced Auditory Serial Addition Test. Methods: We analysed 132 patients (mean age 67 years) undergoing elective cardiac surgery (63.6% valvular, 25% coronary artery bypass grafting and rest mixed procedures) between January and June 2003. We did not include patients with previous history of cognitive impairment, major psychiatric disorders or stroke. Paced Auditory Serial Addition Test was performed before and after surgery (mean, 7 days) and in outpatient follow-up (mean, 4 months). Results: None of the patients suffered a major neurological complication. Mean preoperative Paced Auditory Serial Addition Test score was 27.04±11.05, 25.81±11.83 in immediate postoperative and 27.93±13.11 in follow-up. A significant postoperative neuropsychological dysfunction (test scale decline more than 1 S.D.) was shown in 45.5% of the patients. In 48.8%, decline persisted in follow-up. Valvular surgery and low preoperative Paced Auditory Serial Addition Test score were significant risk factors for immediate postoperative neuropsychological dysfunction. Valvular surgery and female sex were significant in multivariable analysis. Considering follow-up, older age is the only significant risk factor for cognitive impairment. Conclusions: Using a single, quantifiable and easy and quickly applied test such as the Paced Auditory Serial Addition Test, we found an incidence of cognitive decline after cardiac surgery similar to that previously described. Valvular surgery and older age are the main risk factors for neuropsychological dysfunction in our population.

Key Words: Cognitive impairment; Neuropsychological evaluation; Cardiac surgery; Cardiopulmonary bypass


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Cardiac surgery commonly leads to neurological damage, generally due to extracorporeal circulation (ECC). Several other factors such as calcification of the ascending aorta, aortic manipulation and deairing management can also contribute to this type of complication. Symptoms can consist of motor or language deficit, seizures, decreased level of conscience and neuropsychological impairment [1–4]. Neuropsychological impairment has been evaluated by applying multiple tests to estimate attention, immediate and late memory, visual and verbal retention, calculation, information processing speed...etc. According to the different tests applied, postoperative deficits can be detected in up to 90% of patients [1,5,10]. Usually these deficits disappear between 3 and 6 months after procedure, [4,9,10], but in isolated cases, permanent cognitive impairment is identified even after 5 years [11].

Cognitive decline seems to be related to disruptions of white matter pathways that support processing of complex information in geographically distant brain regions [12]. Assessment of cognitive status generally requires a long evaluation time and a complex test battery examination performed by experienced psychometricians. However, the results of these tests can be altered by the use of anaesthetics, post surgical pain or pharmacological therapy required after cardiac surgery.

What is really needed is a simply applied test, concise enough to minimise interpretation subjectivity and accurate enough to correlate with the intensity of cognitive decline after cardiac surgery. It should also be possible for the test to be applied easily and quickly by personnel not specifically trained in psychometrics, such as cardiac surgeons.

PASAT (Paced Auditory Serial Addition Test) is an evaluation system of mild neurological damage used since the 1970's in order to study deterioration secondary to mild traumatic brain injury. In recent years, its use has been extended to other areas in order to explore more selective damage such as that secondary to multiple sclerosis [12–14]. It satisfies many of the assessment criteria recommended for cognitive impairment evaluation after cardiac surgery [7,15,16] and we propose its use in this field.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 5. Conclusions
 References
 
Between January and June of 2003 we evaluated 132 patients who underwent cardiac surgery with ECC. We requested their collaboration in the study and postoperative follow-up. We did not include:

  1. Urgent or emergent surgery.
  2. Cardiac surgery procedures that required use of profound deep hypothermia and circulatory arrest.
  3. Patients with previous neurological diseases such as stroke, seizures and/or coma.
  4. Preoperative cognitive impairment: before their inclusion in the study we performed a Spanish modification of Mini Mental State Examination (MMSE) [17] scored with a maximum of 35. Patients a with preoperative MMSE score under 25 were excluded in order not to include undiagnosed cognitive decline.
  5. Previous psychiatric pathology.
  6. Cerebrovascular disease: more than 50% of unilateral or bilateral carotid stenosis with or without symptoms.
  7. Tumour or cardiac thrombus able to embolize.

Evaluation was designed in 3 steps: preoperative, immediate postoperative and outpatient follow-up. In the preoperative phase clinical history and patient risk factors were reviewed. MMSE and PASAT were performed. In immediate postoperative and follow-up, PASAT was applied.

2.1. PASAT application methodology

Single digits are presented on audiotape every three second. The patient must add each new digit to the one immediately prior to it. Test score is the number of correct sums given. The total number of digits is 60. PASAT has, therefore, an application time of 2 min and patient's learning is impossible. It evaluates: attention, concentration, information processing speed and working memory without causing patient fatigue.

In order to avoid possible subjective variations, we have trained all evaluators (cardiac surgeons) in PASAT application. In postoperative and outpatient follow-up, examiners were blinded to results of previous tests.

Initial objectives of our study were:

  1. Preoperative cognitive evaluation in our population, researching the incidence of neuropsychological impairment after cardiac surgery.
  2. Comparison between results concerning cognitive decline in our population and previous clinical reports and identification of incremental risk factors.
  3. Evaluation of PASAT as an appropriate test to research cognitive impairment after cardiac surgery.

Anesthetic management with midazolam, fentanyl and vecuronium and ECC with moderate hypothermia (32 °C), membrane oxygenator and nonpulsatile perfusion were established.

Statistical analysis was performed with a statistical software package (SPSS 10.0 Operating System). Chi Square or Fisher's Exact test (as appropriate) were used to compare categorical variables and t-test in the continuous means. Group comparisons, before and after surgical procedure, were carried out using the Wilcoxon test. In order to determine risk factors for neuropsychological impairment, a multivariable logistic regression analysis was made. We have considered significant P<0.05.

Neuropsychological impairment was accepted if the postoperative PASAT score decreased by one standard deviation (S.D.) on the baseline score of all patients.

One hundred and thirty two patients (mean age 67±9.67 years; 58.3% men) were enrolled in the study. Only a 6.1% of patients had higher education (more than 13 years of education). Preoperative and intraoperative variables are detailed in Tables 1 and 2. PASAT was carried out preoperatively and in immediate postoperative (7.67±5.38 days) in all patients.


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  		Table 1 Preoperative and intraoperative clinical data. Qualitative variables

 

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  		Table 2 Preoperative and intraoperative clinical data. Quantitative variables

 

   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 5. Conclusions
 References
 
Hospital mortality was 0.7%. One patient died of sepsis secondary to mediastinitis. During follow up 3 patients died, 2 refused to repeat PASAT and 11 patients were lost. Follow up was complete in 87.8% of patients with a mean time of 4.68±2.26 months.

In 60 patients (45.5%), postoperative PASAT score decreased in more than 1 S.D., considered as significant neuropsychological impairment. In this group, in 33 cases (55% of patients) deficit persisted in follow-up.

In univariant analysis, there were significant preoperative risk factors (P<0.05) related with postoperative cognitive impairment: valvular surgery (with a relative risk of 1.5 vs. coronary surgery and confidence interval 95% (1.05–2.1)) and low preoperative PASAT score. The results of univariant analysis are detailed in Tables 2 and 3.


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  		Table 3 Significant risk factors that decreases PASAT score more than 1 S.D. in immediate postoperative

 
Left ventricular dysfunction (with ejection fraction lower than 30%), previous myocardial infarction and unstable post infarction angina were factors that significantly reduced the preoperative PASAT score although none led to a significant cognitive impairment in postoperative. These conclusions correlated low preoperative PASAT score with high surgery risk on the adult EUROSCORE scale.

Significant deterioration in the postoperative PASAT score was observed in 46.5% of the patients with basic studies and only in 25% of those with advanced studies. A high educational level improved significantly preoperative PASAT score in our population (P: 0.06) but it was not an independent protective predictor for neuropsychological impairment after surgery.

In multivariate logistic regression, only female sex (RR 1, 7 CI 95% 0.8–3.4) and valvular surgery were significant incremental risk factors for cognitive impairment in immediate postoperative, and older age (>70 years) in follow up (P<0.001).


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
5. Conclusions
 References
 
Major neurological complications after cardiac surgery have decreased considerably in recent years [1–4,10,18,19]. However, the incidence of postoperative neuropsychological impairment (up to 80% of cases) has undergone little variation. Its occurrence seems to be related with a persistent long-term cognitive decline in cardiac surgery patients [11], and a worsening quality of life [5,20].

Neuropsychological dysfunction after cardiac surgery is related to transitory neuronal metabolism alteration, generated by the use of extracorporeal circulation use. Inflammatory response activation, microscopic air embolism and vasogenic oedema would essentially affect white matter [18]. The clinical expression is cognitive impairment [9–11,21]. Neurobiochemical markers of brain damage (N-acetyl aspartate, neuron-specific enolase and protein S100) showed a significantly higher and longer release [5,8–10,18]. It seems that the cognitive decline is related with subtle reversible damage in white matter interhemispheric pathways [12].

Recent studies confirm the existence of a correlation between decreased scores in PASAT and clinical progression of neurological illnesses such as multiple sclerosis that affect mainly white matter [13,14]. This is why we suggest its use as a valid test to evaluate cognitive decline in cardiac surgery patients. It satisfies the statement of consensus on assessment of neurobehavioral outcomes after cardiac surgery drawn up by the American Thoracic Society (ATS) [16]. PASAT is a simple application test, quick enough to avoid the fatigue of the patient, easily reproducible and with high sensibility and specificity. It evaluates working memory, attention, concentration, calculation and information processing speed, as Lockwood et al. have demonstrated by using positron emission tomography [22], and mapping brain regions activated by PASAT (superior temporal gyri, bifrontal and parietal sites, anterior cingulated and bilateral cerebellar sites). It avoids subjective factors introduced by the evaluator. PASAT learning and the physical effort required for its application are minimal.

In our study, we have compared individual changes in the PASAT result on the preoperative baseline. We have excluded patients with preoperative risk factors for neurological damage and discarded demential syndrome by modified MMSE.

We have tried to avoid variations in PASAT score results described in some studies [23] (up to 23%) due to differences in age, education, intelligence or race, using each individual as a case-control.

Cultural level can modify PASAT score in preoperative evaluation. High educational level could act as a protective factor for cognitive decline. Although these differences were not significant in our population, (85.3% with only basic studies) a postoperative decline was observed in 45.5% of patients with low educational level versus 25% when this was high.

Preoperative left ventricular dysfunction, myocardial infarction and post infarction angina decreased basal PASAT score. This may be related to secondary decreased cerebral flow due to cardiac disease. Correlation between preoperative EUROSCORE surgical risk evaluation and low preoperative PASAT score is probably related to our aged population.

In evaluating preoperative pharmacological treatment, we have not identified any protective factor for cognitive decline [6,24]. It is difficult to determine an individual neuroprotective pharmacological factor in our population because 85% of patients have preoperatively two or more different pharmacological therapies.

Using every patient as a case-control, we have excluded preoperative factors that could modify PASAT results. We have concluded that valvular surgery and low preoperative PASAT score are significant risk factors for cognitive decline in immediate postoperative. Valvular surgery was an independent risk factor, not related with left ventricular dysfunction or atrial arrhythmias. It could be related to air or fat microembolism after opening heart chambers. These microembolisms are easily identified by intraoperative transesophagic echocardiography and transcraneal Doppler. They produce HITS (high-intensity transient signals) that can explain mild neurological impairment after cardiac surgery [19,21]. We have not observed, however, during follow-up, any differences in neuropsychological decline related to different type (biological or mechanical), size or model of valvular prosthesis. This leads us to think that neuropsychological impairment is more closely related with the number of HITS generated during surgical procedure that with thrombogenic or cavitation phenomena produced in patients fitted with a valvular prosthesis.

We have not considered cardiac surgery procedures without ECC in our sample. This does not permit any conclusion related to neuropsychological damage reduction in this group. Previous studies have found a significant reduction in postoperative neuropsychological impairment in myocardial revascularization without ECC [10,25].

Long term cognitive decline in follow up seems related to the degree of cognitive impairment at hospital discharge [7,11] and, in our population, older age is the only significant risk factor for the persistence of these conditions. In this case, cognitive decline related to age could be increased in cardiac surgery patients.

According to what has been stated above, PASAT could be an appropriate test in order to evaluate neuropsychological impairment after cardiac surgery. Arguments in favour are as follows: it properly evaluates cognitive domain, execution time is short (2 min), it is impossible to learn it, requires little physical effort for application and it avoids evaluation subjectivities.

Neuropsychological impairment in our population was similar to results described using more complex test batteries [7,9,18,20,25].

One limitation in our study is that we have not considered patients who underwent cardiac surgery without ECC. In this case we can determine what is the influence of ECC in the aetiology of neurocognitive dysfunction. Arguments against the efficacy of PASAT might be the following: it is only partially free of discriminations for ethnicity, gender and education, it does not permit evaluate spatial concentration and psychomotor speed and it could be affected by postoperative psychological disorders (depression).


   5. Conclusions
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
References
 

  1. Older age is the main predictive factor for postoperative permanent neuropsychological impairment after cardiac surgery.
  2. Valvular surgery leads to a greater cognitive decline than other procedures, possibly due to microembolic events.
  3. PASAT, due to its easy application, good reproducibility and discrimination, could be a simple and practical method of neuropsychological dysfunction evaluation in cardiac surgery patients.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 

  1. Jacobs A, Neveling M, Horst M, Ghaemi M, Kessler J, Eichstaedt H, Rudolf J, Model P, Bonner H, de Vivie ER, Heiss WD. Alterations of neuropsychological function and cerebral glucose metabolism after cardiac surgery are not related only to intraoperative microembolic events. Stroke 1998;29:660–667.[Abstract/Free Full Text]
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  4. Svedjeholm R, Hakanson E, Szabo Z, Vanky F. Neurological injury after surgery for ischemic heart disease: risk factors, outcome and role of metabolic interventions. Eur J Cardiothorac Surg 2001;19:611–618.[Abstract/Free Full Text]
  5. Herrmann M, Ebert AD, Galazky I, Wunderlich MT, Kunz WS, Huth C. Neurobehavioral outcome prediction after cardiac surgery: role of neurobiochemical markers of damage to neuronal and glial brain tissue. Stroke 2000;31:645–650.[Abstract/Free Full Text]
  6. Murkin JM. Attenuation of neurologic injury during cardiac surgery. Ann Thorac Surg 2001;72:S1838–S1844.[Abstract/Free Full Text]
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  8. Georgiadis D, Berger A, Kowatschev E, Lautenschlager C, Borner A, Lindner A, Schulte-Mattler W, Zerkowski HR, Zierz S, Deufel T. Predictive value of S-100 and neuron-specific enolase serum levels for adverse neurologic outcome after cardiac surgery. J Thorac Cardiovasc Surg 2000;119:138–147.[Abstract/Free Full Text]
  9. Mullges W, Babin-Ebel J, Reents W, Toyka KV. Cognitive performance after coronary bypass grafting: A follow up study. Neurology 2002;59:741–743.[Abstract/Free Full Text]
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  11. Newman MF, Kirchner JL, Phillips-Bute B, Gaver V, Grocott H, Jones RH, Mark DB, Reves JG, Blumenthal JA. Neurological Outcome Research Group and the Cardiothoracic Anesthesiology Research Endeavors Investigators. Longitudinal assessment of neurocognitive function after coronary-artery bypass surgery. N Engl J Med 2001;344:395–402.[Abstract/Free Full Text]
  12. Snyder PJ, Cappelleri JC. Information processing speed deficits may be better correlated with the extent of white matter sclerotic lesions in multiple sclerosis than previously suspected. Brain Cogn 2001;46:279–284.[Medline]
  13. Fisk JD, Archibald CJ. Limitations of the Paced Auditory Serial Addition Test as a measure of working memory in patients with multiple sclerosis. J Int Neuropsychol Soc 2001;7:363–372.[CrossRef][Medline]
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  15. Mahanna EP, Blumenthal JA, White WD, Croughwell ND, Clancy CP, Smith LR, Newman MF. Defining neuropsychological dysfunction after coronary artery bypass grafting. Ann Thorac Surg 1996;61:1342–1347.[Abstract/Free Full Text]
  16. Murkin JM, Newman SP, Stump DA, Blumenthal JA. Statement of consensus on assessment of neurobehavioral outcomes after cardiac surgery. Ann Thorac Surg 1995;59:1289–1295.[Free Full Text]
  17. Lobo A, Ezquerra J, Gomez Burgada F, Sala JM, Seva Diaz A. Cognocitive mini-test (a simple practical test to detect intellectual changes in medical patients). Actas LusoEsp Neurol Psiquiatr Cienc Afines 1979;7:189–202.
  18. Bendszus M, Reents W, Franke D, Mullges W, Babin-Ebell J, Koltzenburg M, Warmuth-Metz M, Solymori L. Brain damage after coronary artery bypass. Arch Neurol 2002;59:1090–1095.[Abstract/Free Full Text]
  19. Borger MA, Ivanov J, Weisel RD, Rao V, Peniston CM. Stroke during coronary bypass surgery: principal role of cerebral macroemboli. Eur J Cardio thorac Surg 2001;19:627–632.[Abstract/Free Full Text]
  20. Newman MF, Grocott HP, Mathew JP, White WD, Landolfo K, Reves JG, Laskowitz DT, Mark DB, Blumenthal JA. CARE. Report of the substudy assessing the impact of neurocognitive function on quality of life 5 years after cardiac surgery. Stroke 2001;32:2874–2881.[Abstract/Free Full Text]
  21. Deklunder G, Roussel M, Lecroart JL, Prat A, Gautier C. Microemboli in cerebral circulation and alteration of cognitive abilities in patients with mechanical prosthetic heart valves. Stroke 1998;29:1821–1826.[Abstract/Free Full Text]
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This Article
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Salvatore Di Stefano
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Right arrow Articles by Carrascal, Y.
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Related Collections
Right arrow Cerebral protection
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