Postoperative cognitive dysfunction (POCD) is a mild form of perioperative ischemic brain injury, which emerges as memory decline, decreased attention, and decreased concentration during several months, or even years, after surgery. Here we present results of our three neuropsychological studies, which overall included 145 patients after on-pump operations. We found that the auditory memory span test (digit span) was more effective as a tool for registration of POCD, in comparison with the word-list learning and story-learning tests. Nonverbal memory or visuoconstruction tests were sensitive to POCD in patients after intraoperative opening of cardiac chambers with increased cerebral air embolism. Psychomotor speed tests (digit symbol, or TMT A) registered POCD, which was characteristic for elderly atherosclerotic patients. Finally, we observed that there were significant effects of the order of position of a test on the performance on this test. For example, the postoperative performance on the core tests (digit span and digit symbol) showed minimal impairment when either of these tests was administered at the beginning of testing. Overall, our data shows that the selection of tests, and the order of which these tests are administered, may considerably influence the results of studies of POCD. 1. Introduction Postoperative cognitive dysfunction (POCD) is a mild form of perioperative ischemic brain injury, which emerges predominantly as memory decline during several months, or even years after surgery [1–5]. In addition, patients commonly report decreased concentration, attention span, and psychomotor speed. Both patients and spouses of patients notice postoperative memory decline after the first year after operation [3]. Negative effects on driving abilities during several months after uncomplicated cardiac surgeries were registered [6]. Some researchers include a broader spectrum of disorders around the term “postoperative cognitive dysfunction”—these disorders may include perioperative ischemic brain damage, brain death, delirium, stroke, and transitory ischemic attack [5]. Multiple neuropsychological studies confirm a decline in the performance of cognitive tests in the majority of patients during the first week after cardiac surgery and in about 30–40% of patients in 1–3 months after surgery in comparison with preoperative testing [review: [7]]. In young patients, cognitive function tends to be restored to its preoperative levels, in about 6–12 months after surgery [8–12], and there is no association between POCD and risk of dementia, in this young
References
[1]
K. A. Sotaniemi, H. Mononen, and T. E. Hokkanen, “Long-term cerebral outcome after open-heart surgery. A five-year neuropsychological follow-up study,” Stroke, vol. 17, no. 3, pp. 410–416, 1986.
[2]
G. Vingerhoets, G. de Soete, and C. Jannes, “Subjective complaints versus neuropsychological test performance after cardiopulmonary bypass,” Journal of Psychosomatic Research, vol. 39, no. 7, pp. 843–853, 1995.
[3]
C. Bergh, M. B？ckstr？m, H. J？nsson, L. Havinder, and P. Johnsson, “In the eye of both patient and spouse: memory is poor 1 to 2 years after coronary bypass and angioplasty,” Annals of Thoracic Surgery, vol. 74, no. 3, pp. 689–693, 2002.
[4]
S. Newman, J. Stygall, S. Hirani, S. Shaefi, and M. Maze, “Postoperative cognitive dysfunction after noncardiac surgery: a systematic review,” Anesthesiology, vol. 106, no. 3, pp. 572–590, 2007.
[5]
T. L. Tsai, L. P. Sands, and J. M. Leung, “An update on postoperative cognitive dysfunction,” Advances in Anesthesia, vol. 28, pp. 269–284, 2010.
[6]
E. Ahlgren, A. Lundqvist, A. Nordlund, C. Aren, and H. Rutberg, “Neurocognitive impairment and driving performance after coronary artery bypass surgery,” European Journal of Cardio-thoracic Surgery, vol. 23, no. 3, pp. 334–340, 2003.
[7]
L. A. Bokeriia, E. Z. Golukhova, A. G. Polunina, D. M. Davydov, and A. V. Begachev, “Neural correlates of cognitive dysfunction after cardiac surgery,” Brain Research Reviews, vol. 50, no. 2, pp. 266–274, 2005.
[8]
E. P. Mahanna, J. A. Blumenthal, W. D. White et al., “Defining neuropsychological dysfunction after coronary artery bypass grafting,” Annals of Thoracic Surgery, vol. 61, no. 5, pp. 1342–1347, 1996.
[9]
M. Herrmann, A. D. Ebert, I. Galazky, M. T. Wunderlich, W. S. Kunz, and C. Huth, “Neurobehavioral outcome prediction after cardiac surgery: role of neurobiochemical markers of damage to neuronal and glial brain tissue,” Stroke, vol. 31, no. 3, pp. 645–650, 2000.
[10]
M. J. Neville, J. Butterworth, R. L. James, J. W. Hammon, and D. A. Stump, “Similar neurobehavioral outcome after valve or coronary artery operations despite differing carotid embolic counts,” Journal of Thoracic and Cardiovascular Surgery, vol. 121, no. 1, pp. 125–136, 2001.
[11]
M. F. Newman, J. L. Kirchner, B. Phillips-Bute et al., “Longitudinal assessment of neurocognitive function after coronary-artery bypass surgery,” The New England Journal of Medicine, vol. 344, no. 6, pp. 395–402, 2001.
[12]
O. A. Selnes, R. M. Royall, M. A. Grega, J. Borowicz L.M., S. Quashey, and G. M. McKhann, “Cognitive changes 5 years after coronary artery bypass grafting: is there evidence of late decline?” Archives of Neurology, vol. 58, no. 4, pp. 598–604, 2001.
[13]
J. Steinmetz, K. B. Christensen, T. Lund, N. Lohse, and L. S. Rasmussen, “Long-term consequences of postoperative cognitive dysfunction,” Anesthesiology, vol. 110, no. 3, pp. 548–555, 2009.
[14]
M. F. Newman, H. P. Grocott, J. P. Mathew et al., “Report of the substudy assessing the impact of neurocognitive function on quality of life 5 years after cardiac surgery,” Stroke, vol. 32, no. 12, pp. 2874–2881, 2001.
[15]
D. N. F. Harris, A. Oatridge, D. Dob, P. L. C. Smith, K. M. Taylor, and G. M. Bydder, “Cerebral swelling after normothermic cardiopulmonary bypass,” Anesthesiology, vol. 88, no. 2, pp. 340–345, 1998.
[16]
A. Jacobs, M. Neveling, M. Horst et al., “Alterations of neuropsychological function and cerebral glucose metabolism after cardiac surgery are not related only to intraoperative microembolic events,” Stroke, vol. 29, no. 3, pp. 660–667, 1998.
[17]
R. E. Anderson, T.-Q. Li, T. Hindmarsh, G. Settergren, and J. Vaage, “Increased extracellular brain water after coronary artery bypass grafting is avoided by off-pump surgery,” Journal of Cardiothoracic and Vascular Anesthesia, vol. 13, no. 6, pp. 698–702, 1999.
[18]
M. Bendszus, W. Reents, D. Franke et al., “Brain damage after coronary artery bypass grafting,” Archives of Neurology, vol. 59, no. 7, pp. 1090–1095, 2002.
[19]
L. Restrepo, R. J. Wityk, M. A. Grega et al., “Diffusion- and perfusion-weighted magnetic resonance imaging of the brain before and after coronary artery bypass grafting surgery,” Stroke, vol. 33, no. 12, pp. 2909–2915, 2002.
[20]
S. C. Knipp, N. Matatko, H. Wilhelm et al., “Evaluation of brain injury after coronary artery bypass grafting. A prospective study using neuropsychological assessment and diffusion-weighted magnetic resonance imaging,” European Journal of Cardio-Thoracic Surgery, vol. 25, no. 5, pp. 791–800, 2004.
[21]
E. Stolz, T. Gerriets, A. Kluge, W.-P. Kl？vekorn, M. Kaps, and G. Bachmann, “Diffusion-weighted magnetic resonance imaging and neurobiochemical markers after aortic valve replacement,” Stroke, vol. 35, no. 4, pp. 888–892, 2004.
[22]
T. F. Floyd, P. N. Shah, C. C. Price et al., “Clinically silent cerebral ischemic events after cardiac surgery: their incidence, regional vascular occurrence, and procedural dependence,” Annals of Thoracic Surgery, vol. 81, no. 6, pp. 2160–2166, 2006.
[23]
J. D. Salazar, R. J. Wityk, M. A. Grega et al., “Stroke after cardiac surgery: short- and long-term outcomes,” Annals of Thoracic Surgery, vol. 72, no. 4, pp. 1195–1201, 2001.
[24]
R. J. Wityk, M. A. Goldsborough, A. Hillis et al., “Diffusion- and perfusion-weighted brain magnetic resonance imaging in patients with neurologic complications after cardiac surgery,” Archives of Neurology, vol. 58, no. 4, pp. 571–576, 2001.
[25]
D. Barbut, Y.-W. Lo, J. P. Gold et al., “Impact of embolization during coronary artery bypass grafting on outcome and length of stay,” Annals of Thoracic Surgery, vol. 63, no. 4, pp. 998–1002, 1997.
[26]
S. Sylivris, C. Levi, G. Matalanis et al., “Pattern and significance of cerebral microemboli during coronary artery bypass grafting,” Annals of Thoracic Surgery, vol. 66, no. 5, pp. 1674–1678, 1998.
[27]
L. A. Bokeriia, E. Z. Golukhova, and A. G. Polunina, “Postoperative delirium in cardiac surgery: microembolic load is an important factor,” Annals of Thoracic Surgery, vol. 88, no. 1, pp. 349–350, 2009.
[28]
S. J. Fearn, R. Pole, K. Wesnes, E. B. Faragher, T. L. Hooper, and C. N. McCollum, “Cardiopulmonary support and physiology. Cerebral injury during cardiopulmonary bypass: emboli impair memory,” Journal of Thoracic and Cardiovascular Surgery, vol. 121, no. 6, pp. 1150–1160, 2001.
[29]
J. D. Lee, S. J. Lee, W. T. Tsushima et al., “Benefits of off-pump bypass on neurologic and clinical morbidity: a prospective randomized trial,” Annals of Thoracic Surgery, vol. 76, no. 1, pp. 18–26, 2003.
[30]
J. Stygall, S. P. Newman, G. Fitzgerald et al., “Cognitive change 5 years after coronary artery bypass surgery,” Health Psychology, vol. 22, no. 6, pp. 579–586, 2003.
[31]
R. S. D'Agostino, L. G. Svensson, D. J. Neumann, H. H. Balkhy, W. A. Williamson, and D. M. Shahian, “Screening carotid ultrasonography and risk factors for stroke in coronary artery surgery patients,” Annals of Thoracic Surgery, vol. 62, no. 6, pp. 1714–1723, 1996.
[32]
D. J. Blacker, K. D. Flemming, and E. F. M. Wijdicks, “Risk of ischemic stroke in patients with symptomatic vertebrobasilar stenosis undergoing surgical procedures,” Stroke, vol. 34, no. 11, pp. 2659–2663, 2003.
[33]
Y. M. Ganushchak, E. J. Fransen, C. Visser, D. S. De Jong, and J. G. Maessen, “Neurological complications after coronary artery bypass grafting related to the performance of cardiopulmonary bypass,” Chest, vol. 125, no. 6, pp. 2196–2205, 2004.
[34]
L. R. Caplan and M. Hennerici, “Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke,” Archives of Neurology, vol. 55, no. 11, pp. 1475–1482, 1998.
[35]
T. Omae, O. Mayzel-Oreg, F. Li, C. H. Sotak, and M. Fisher, “Inapparent hemodynamic insufficiency exacerbates ischemic damage in a rat microembolic stroke model,” Stroke, vol. 31, no. 10, pp. 2494–2499, 2000.
[36]
G. Orlandi, S. Fanucchi, S. Gallerini et al., “Impaired clearance of microemboli and cerebrovascular symptoms during carotid stenting procedures,” Archives of Neurology, vol. 62, no. 8, pp. 1208–1211, 2005.
[37]
A. Parolari, M. Camera, F. Alamanni et al., “Systemic inflammation after on-pump and off-pump coronary bypass surgery: a one-month follow-up,” Annals of Thoracic Surgery, vol. 84, no. 3, pp. 823–828, 2007.
[38]
E. F. Bruggemans, “Cognitive dysfunction after cardiac surgery: pathophysiological mechanisms and preventive strategies,” Netherlands Heart Journal, vol. 21, pp. 70–73, 2013.
[39]
M. J. Koessler, R. Fabiani, H. Hamer, and R. P. Pitto, “The clinical relevance of embolic events detected by transesophageal echocardiography during cemented total hip arthroplasty: a randomized clinical trial,” Anesthesia and Analgesia, vol. 92, no. 1, pp. 49–55, 2001.
[40]
S. Koch, A. Forteza, C. Lavernia et al., “Cerebral fat microembolism and cognitive decline after hip and knee replacement,” Stroke, vol. 38, no. 3, pp. 1079–1081, 2007.
[41]
Y.-H. Kim, J.-S. Kim, K.-S. Hong, Y.-J. Kim, and J.-H. Kim, “Prevalence of fat embolism after total knee arthroplasty performed with or without computer navigation,” Journal of Bone and Joint Surgery A, vol. 90, no. 1, pp. 123–128, 2008.
[42]
M. A. Mirski, A. V. Lele, L. Fitzsimmons, and T. J. K. Toung, “Diagnosis and treatment of vascular air embolism,” Anesthesiology, vol. 106, no. 1, pp. 164–177, 2007.
[43]
L. Dube, C. Soltner, S. Daenen, J. Lemarie, P. Asfar, and P. Alquier, “Gas embolism: an exceptional complication of radial arterial catheterization,” Acta Anaesthesiologica Scandinavica, vol. 48, no. 9, pp. 1208–1210, 2004.
[44]
M. W. Sowell, C. L. Lovelady, B. G. Brogdon, and C. H. Wecht, “Infant death due to air embolism from peripheral venous infusion,” Journal of Forensic Sciences, vol. 52, no. 1, pp. 183–188, 2007.
[45]
L. S. Rasmussen, K. Larsen, P. Houx, L. T. Skovgaard, C. D. Hanning, and J. T. Moller, “The assessment of postoperative cognitive function,” Acta Anaesthesiologica Scandinavica, vol. 45, no. 3, pp. 275–289, 2001.
[46]
L. A. Bokeria, E. Z. Golukhova, A. G. Polunina, and N. Y. U. Breskina, “Methods of evaluation of neurological outcomes of cardiac surgery,” GrudnaIa I Serdechno-SosudIstaIa KhIrurgIa, vol. 2, pp. 8–14, 2005.
[47]
J. A. Blumenthal, E. P. Mahanna, D. J. Madden, W. D. White, N. D. Croughwell, and M. F. Newmann, “Methodological issues in the assessment of neuropsychologic function after cardiac surgery,” Annals of Thoracic Surgery, vol. 59, no. 5, pp. 1345–1350, 1995.
[48]
J. E. Arrowsmith, H. P. Grocott, J. G. Reves, and M. F. Newman, “Central nervous system complications of cardiac surgery,” British Journal of Anaesthesia, vol. 84, no. 3, pp. 378–393, 2000.
[49]
D. Van Dijk, A. M. A. Keizer, J. C. Diephuis, C. Durand, L. J. Vos, and R. Hijman, “Neurocognitive dysfunction after coronary artery bypass surgery: a systematic review,” Journal of Thoracic and Cardiovascular Surgery, vol. 120, no. 4, pp. 632–639, 2000.
[50]
P. Slade, P. Sanchez, B. Townes, and G. S. Aldea, “The use of neurocognitive tests in evaluating the outcome of cardiac surgery: some methodologic considerations,” Journal of Cardiothoracic and Vascular Anesthesia, vol. 15, no. 1, pp. 4–8, 2001.
[51]
A. Collie, D. G. Darby, M. G. Falleti, B. S. Silbert, and P. Maruff, “Determining the extent of cognitive change after coronary surgery: a review of statistical procedures,” Annals of Thoracic Surgery, vol. 73, no. 6, pp. 2005–2011, 2002.
[52]
S. M. Browne, P. W. Halligan, D. T. Wade, and D. P. Taggart, “Cognitive performance after cardiac operation: implications of regression toward the mean,” Journal of Thoracic and Cardiovascular Surgery, vol. 117, no. 3, pp. 481–485, 1999.
[53]
J. B. Dijkstra and J. Jolles, “Postoperative cognitive dysfunction versus complaints: a discrepancy in long-term findings,” Neuropsychology Review, vol. 12, no. 1, pp. 1–13, 2002.
[54]
J. M. Murkin, J. S. Martzke, A. M. Buchan, C. Bentley, and C. J. Wong, “A randomized study of the influence of perfusion technique and pH management strategy in 316 patients undergoing coronary artery bypass surgery. II. Neurologic and cognitive outcomes,” Journal of Thoracic and Cardiovascular Surgery, vol. 110, no. 2, pp. 349–362, 1995.
[55]
A. G. Polunina, “Selection of neurocognitive tests and outcomes of cardiac surgery trials,” Annals of Thoracic Surgery, vol. 85, no. 1, p. 362, 2008.
[56]
L. A. Bokeriia, E. Z. Golukhova, N. Y. Breskina et al., “Asymmetric cerebral embolic load and postoperative cognitive dysfunction in cardiac surgery,” Cerebrovascular Diseases, vol. 23, no. 1, pp. 50–56, 2007.
[57]
E. Z. Golukhova, A. G. Polunina, N. P. Lefterova, and A. V. Begachev, “Electroencephalography as a tool for assessment of brain ischemic alterations after open heart operations,” Stroke Research and Treatment, vol. 2011, Article ID 980873, 14 pages, 2011.
[58]
E. Z. Golukhova, A. G. Polunina, N. P. Lefterova, O. D. Morelli, and A. V. Begachev, “Electroencephalography as a tool for assessment of brain ischemic alteration after coronary artery bypass grafting,” Kreativnaya Kardiologia, vol. 1, pp. 107–122, 2012.
[59]
Y. Filimonenko and V. Timofeev, Manual for the Russian Version of the Wechsler Adult Intelligence Scale, Adapted in 1995, Imaton, Sankt-Peterburg, Russia, 1995.
[60]
M. F. Folstein, S. Folstein, and P. R. McHugh, “Mini-mental state: a practical method for grading the cognitive state of patients for the clinician,” Psychiatry Research, vol. 12, p. 189, 1975.
[61]
S. N. Mosolov, Scales of Psychometric Evaluation of Symptoms of Schizophrenia and Conception of Positive and Negative Disturbances, ZAO: “Noviy zcvet”, Moscow,Russia, 2001.
[62]
I. Sánchez-Cubillo, J. A. Periá？ez, D. Adrover-Roig, et al., “Construct validity of the Trail Making Test: role of task-switching, working memory, inhibition/interference control, and visuomotor abilities,” Journal of the International Neuropsychological Society, vol. 15, no. 3, pp. 438–450, 2009.
[63]
T. A. Salthouse, “What cognitive abilities are involved in trail-making performance?” Intelligence, vol. 39, no. 4, pp. 222–232, 2011.
[64]
G. S. Weinstein, “Left hemispheric strokes in coronary surgery: implications for end-hole aortic cannulas,” Annals of Thoracic Surgery, vol. 71, no. 1, pp. 128–132, 2001.
[65]
L. S. Rasmussen, B. Sperling, H. H. Abildstr？m, and J. T. Moller, “Neuron loss after coronary artery bypass detected by SPECT estimation of benzodiazepine receptors,” Annals of Thoracic Surgery, vol. 74, no. 5, pp. 1576–1580, 2002.
[66]
R. R. Leker, A. Pollak, O. Abramsky, and T. Ben-Hur, “Abundance of left hemispheric embolic strokes complicating coronary angiography and PTCA,” Journal of Neurology Neurosurgery and Psychiatry, vol. 66, no. 1, pp. 116–117, 1999.
[67]
C. Foerch, B. Misselwitz, M. Sitzer, K. Berger, H. Steinmetz, and T. Neumann-Haefelin, “Difference in recognition of right and left hemispheric stroke,” The Lancet, vol. 366, no. 9483, pp. 392–393, 2005.
[68]
H. Naess, U. Waje-Andreassen, L. Thomassen, and K.-M. Myhr, “High incidence of infarction in the left cerebral hemisphere among young adults,” Journal of Stroke and Cerebrovascular Diseases, vol. 15, no. 6, pp. 241–244, 2006.
[69]
V. S. Hedna, A. N. Bodhit, and S. Ansari, “Hemispheric differences in ischemic stroke: is left-hemisphere stroke more common?” The Journal of Clinical Neurology, vol. 9, no. 2, pp. 97–102, 2013.
[70]
D. N. Atochin, J. C. Murciano, Y. Gürsoy-？zdemir et al., “Mouse model of microembolic stroke and reperfusion,” Stroke, vol. 35, no. 9, pp. 2177–2182, 2004.
[71]
M. A. Borger, C. M. Peniston, R. D. Weisel, M. Vasiliou, R. E. A. Green, and C. M. Feindel, “Neuropsychologic impairment after coronary bypass surgery: effect of gaseous microemboli during perfusionist interventions,” Journal of Thoracic and Cardiovascular Surgery, vol. 121, no. 4, pp. 743–749, 2001.
[72]
M. J. Andrew, R. A. Baker, J. Bennetts, A. C. Kneebone, and J. L. Knight, “A comparison of neuropsychologic deficits after extracardiac and intracardiac surgery,” Journal of Cardiothoracic and Vascular Anesthesia, vol. 15, no. 1, pp. 9–14, 2001.
[73]
J. Bucerius, J. F. Gummert, M. A. Borger et al., “Stroke after cardiac surgery: a risk factor analysis of 16,184 consecutive adult patients,” Annals of Thoracic Surgery, vol. 75, no. 2, pp. 472–478, 2003.
[74]
U. Boeken, J. Litmathe, P. Feindt, and E. Gams, “Neurological complications after cardiac surgery: risk factors and correlation to the surgical procedure,” Thoracic and Cardiovascular Surgeon, vol. 53, no. 1, pp. 33–36, 2005.
[75]
I. Korn-Lubetzki, I. Steiner, A. Oren, R. Tauber, B. Steiner-Birmanns, and D. Bitran, “The possible risk for strokes complicating cardiac surgery in patients with intraoperative hypothermia,” Cerebrovascular Diseases, vol. 30, no. 6, pp. 602–605, 2010.
[76]
I. Korn-Lubetzki, A. Oren, E. Asher et al., “Strokes after cardiac surgery: mostly right hemispheric ischemic with mild residual damage,” Journal of Neurology, vol. 254, no. 12, pp. 1708–1713, 2007.
[77]
V. I. Chernov, N. Y. Efimova, I. Y. Efimova, S. D. Akhmedov, and Y. B. Lishmanov, “Short-term and long-term cognitive function and cerebral perfusion in off-pump and on-pump coronary artery bypass patients,” European Journal of Cardio-thoracic Surgery, vol. 29, no. 1, pp. 74–81, 2006.
[78]
G. E. Swan, A. LaRue, D. Carmelli, T. E. Reed, and R. R. Fabsitz, “Decline in cognitive performance in aging twins: heritability and biobehavioral predictors from the National Heart, Lung, and Blood Institute Twin Study,” Archives of Neurology, vol. 49, no. 5, pp. 476–481, 1992.
[79]
O. L. Lopez, W. J. Jagust, C. Dulberg et al., “Risk factors for mild cognitive impairment in the cardiovascular health study cognition study,” Archives of Neurology, vol. 60, no. 10, pp. 1394–1399, 2003.
[80]
K. P. Rankin, G. S. Kochamba, K. B. Boone, D. B. Petitti, and J. G. Buckwalter, “Presurgical cognitive deficits in patients receiving coronary artery bypass graft surgery,” Journal of the International Neuropsychological Society, vol. 9, no. 6, pp. 913–924, 2003.
[81]
O. A. Selnes, M. A. Grega, L. M. Borowicz Jr. et al., “Cognitive outcomes three years after coronary artery bypass surgery: a comparison of on-pump coronary artery bypass graft surgery and nonsurgical controls,” Annals of Thoracic Surgery, vol. 79, no. 4, pp. 1201–1209, 2005.
