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Ann Thorac Surg 2000;69:1162-1166
© 2000 The Society of Thoracic Surgeons
a Department of Cardiac Surgery, Herzzentrum, Universität Leipzig, Leipzig, Germany
Address reprint requests to Dr Diegeler, Department of Cardiac Surgery, Herzzentrum, Universität Leipzig, Russenstraße 19, D-04289 Leipzig, Germany
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Abstract |
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Methods. Forty patients were randomized in 2 groups (20 conventional and 20 off-pump CABG). Neurocognitive status was assessed preoperatively and postoperatively. Venous serum levels of S-100 protein were measured before and after coronary operation, HITS were measured in the middle cerebral artery during the operation.
Results. The median value of HITS was 394.5 (0 to 2217) in the conventional versus 11 (0 to 50) in the off-pump group, p less than 0.0001 (Table 1). Postoperative S-100 serum levels were: 3.76 (0.13 to 11.2) µg/L (conventional) versus 0.13 (0.04 to 1.01) µg/L (off-pump), p less than 0.0001. Postoperative cognitive testing showed significantly different results with a postoperative impairment of 90% of the patients in the conventional group versus no impairment in the off-pump group.
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Introduction |
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TopAbstractIntroductionMaterial and methodsResultsCommentReferences |
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Different authors have hypothesized that there exists an association between size and quality of cerebral emboli [4]. Thus, ischemic stroke appears to be secondary to particular macroemboli arising from calcified vessels, especially in the aortic arch. As for cerebral microemboli, several studies using transcranial Doppler echography have reported that there is a correlation between microemboli count and neuropsychologic outcome [5–7]. Changes in postoperative neurocognitive outcome have been related to air embolisms arising from the CPB circuit. Arterial line filtration has been shown to reduce both microemboli and neuropsychological impairment [8]. But despite the continuing evolution in CPB techniques and management, this problem has not been eliminated completely so far. The apparently mild and transient character of neurocognitive dysfunction has to be reassessed since long-term studies have demonstrated that this partially persists [9].
Recently, direct myocardial revascularization without CPB (off-pump operation), in order to reduce the surgical invasiveness, has regained interest [10–12]. It is now used more, since new techniques for exposure of the target coronary artery and various devices have become available. Cardiopulmonary bypass and aortic canulation are not applied with this technique, and therefore the incidence of neuropsychologic dysfunction that may be related to CPB technique should be reduced. The aim of the current study was to investigate the impact of CPB on neuropsychological function using different neuromonitoring methods in conventional and off-pump coronary operation.
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsCommentReferences |
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Anesthesia
Nordazepam and midazolam served as premedication. For induction, sufentanyl, disoprivan and pancuronium were used, anesthesia was maintained with sufentanyl and disoprivan using a standardized protocol. One radial or femoral artery catheter, one peripheral and a triple lumen central venous line were inserted.
Cardiopulmonary bypass
Conventional CABG was performed with a Stöckert S3 roller pump (Stöckert, Munich, Germany), membrane oxygenators (Maxima forte, Medtronic, Minneapolis, MN) and a 40 µm arterial blood filter (Medtronic). A visually controllable microbubble sensor was interposed in the arterial line in order to stop the blood flow when detecting microbubbles greater than 30 µm. Moderate hypothermia (32° C) and alpha-stat management were applied. Systemic blood pressure was regulated pharmacologically to maintain mean arterial pressures above 50 mmHg. Surgical and anesthetic staff were blinded to the results of transcranial Doppler ultrasound (TCD) monitoring during the procedure.
Off-pump technique
Off-pump operation was usually applied to patients having isolated coronary artery disease and is suitable for both, on-pump or off-pump techniques. The exclusion criteria for off-pump operation, and for the study in general, have been as follows: acute ischemic myocardial damage (acute vascular occlusion), unstable angina pectoris, ejection fraction less than 30% and concomitant diseases related to a left-ventricular valve or to the ascending aorta.
The surgical technique includes intraoperative exposition and immobilization of the target vessels with commercially available stabilization devices. A temporary occlusion of the target vessel at the anastomosis was achieved by proximal and distal snares. Anastomosis between the graft and coronary artery was performed similar to the conventional technique. The proximal anastomosis of the vein graft was performed while the aorta was partially clamped.
Intraoperative transcranial Doppler monitoring
A 2-MHz pulsed-wave TCD-System (Multi Dop X4, DWL Elektronische Systeme; Sipplingen, Germany) was used for continuous monitoring of middle cerebral artery blood flow in two depths between 42 and 72 mm simultaneously (multirange principle). The probes were fixed transtemporally above the right and left zygomatic arch using a spectacle frame. Embolic signals were defined as transient high-amplitude signals (HITS) occurring time-shifted in both measured depths over the background signal. The intraoperative monitoring was performed by one physician, who subsequently reviewed and verified the data.
S-100 analytical method
The intracellular calcium binding protein S-100 is a dimeric protein with alpha (
) or beta (ß) subunits. The ß subunit is contained in glial and Schwann cells, and is highly brain specific. Increased levels of S-100 in serum or cerebrospinal fluid have been reported as a very sensitive marker for diffuse minor or major brain injury [13–15].
Venous serum was taken before and immediately after the operation, as well as at 6, 12, 24, and 48 hours postoperatively, in all patients. The samples were kept at -78° C until measuring. The serum concentration of S-100 protein was measured using an Immunoluminometric Assay Kit (LIA; Byk Sangtec Diagnostica, Dietzenbach, Germany) containing a monoclonal antibody detecting S-100ß dimeric isoform in duplicates (coefficient of variation between 1.1 and 6.4). The kit allowed a analytical sensitivity of 0.02 µg/L. A concentration of greater than 0.12 µg/L was considered to be pathologically elevated [16].
Neurologic and neuropsychologic assessment
Patients were examined preoperatively and postoperatively using the following methods: (1) Canadian Stroke Scale (CSS), a quantitative motor function scale (normal value: 15 points); (2) a quantitative, standardized psychiatric assessment (normal value: 17.5 points); and (3) Syndrom Kurz Test (SKT), a rating scale consisting of nine consecutive subtests to examine patient performance in cognitive function of memory and attention [17, 18]. Normal cognitive range varies from 0 to 4 points. Examination was performed 1 day before and on the seventh postoperative day. For the SKT, different kits were used to avoid learning effects.
Statistics
Computerized statistical analysis was performed using SPSS (SPSS, Inc, Chicago, IL) for Windows. Clinical data and results are given as mean ± standard deviation, and HITS and biochemical data as mean ± standard deviation, median, and interquartile range. For group differences, the Mann-Whitney U-test and 
2-test were used. Correlation between S-100 levels, scores, HITS, and clinical data were calculated using the Spearman correlation coefficient, and a p value less than 0.05 was considered statistically significant.
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Results |
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The median number of HITS in group A was 394.5 (0 to 2217) versus 11 (0 to 50) in group B (Fig 1; p < 0.0001). Five patients had fewer than 200 HITS, 10 patients showed 200 to 800 HITS, and in 4 patients 800 to 1200 HITS were measured. One patient had more than 2200 HITS and sustained a transient neuropsychiatric syndrome. In group B, total emboli count per patient did not exceed 50. The distribution was as follows: 5 patients with fewer than 10 HITS, 9 patients with 10 to 20 HITS, and 6 patients with 21 to 50 HITS. In group A, there was a significant correlation found between the number of HITS and SKT according to the preoperative and postoperative score differences (r = 0.69, p < 0.002), but there was no correlation between HITS and quantitative psychiatric assessment or CSS score.
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Comment |
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TopAbstractIntroductionMaterial and methodsResultsCommentReferences |
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In comparison to previous studies [6–8], high numbers of HITS were found in the conventional group. In the present study a spectacle frame with two probes detecting the median cerebri artery on both sides have been used, whereas different authors used single probes for TCD monitoring, or did not specify whether one or two probes were used. We found the maximum number of HITS (2200) in 1 patient who showed a transient neuropsychiatric syndrome after conventional CABG operation. All remaining patients in the conventional group did not exceed 800 embolic signals. On the basis of the present data, it is still not clear whether neuropsychiatric impairments follow a threshold type, as suggested by Clark and colleagues [7], or a linear relationship to the quantity of HITS, to be pathologically effective. Another interesting finding was that the cannulation and decannulation procedures of the ascending aorta caused an increased onset of HITS, as well as declamping, which was more pronounced in the conventional group. A major problem is lack of information about the size of the embolic particle, which cannot be calculated by the methods used. However, if one compares the present quantitative findings of HITS in conventional versus off-pump CABG, a strong association between microemboli and CPB is found. Over the entire postoperative period, S-100 serum concentration was considerably higher in the CPB group than in the off-pump group. S-100 serum concentration in the off-pump group also showed slightly elevated levels in the immediate postoperative period although without measurable consequences on the clinical outcome. This may be due to the general traumatic influence of the surgical procedure [23]. Nevertheless, a precise relationship of elevated S-100 levels to cognitive dysfunction could not be demonstrated in the present study. We found no correlation to S-100 serum level in the patient who had the highest embolic load and the neuropsychiatric syndrome. Even the patient who had a stroke did not show extraordinary high S-100 values. Furthermore, in another patient, the highest postoperative S-100 serum level (11.2 µg/L) was not correlated to cognitive impairment or outstanding embolic load (Fig 3). If compared, both surgical groups off-pump patients had a very slight early increase postoperatively but this was only a slight increase beyond the pathologic level went back to normal at about 6 hours postoperatively. In the conventional group, S-100 levels were raised until 2 days after the procedure. This leads to the question of whether pathologically elevated postoperative S-100 serum levels are directly caused by central nervous system cell damage, or more related to CPB exposure and cooling of the blood. The latter has to be verified under normothermic conditions.
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The impact of neuropsychologic impairment on psychosocial conditions on convalescing patients, may be estimated, but could not be clarified by the present study. This must be evaluated further through long-term follow-up.
Despite some limitations due to the design, the present study demonstrates a significant difference between conventional and off-pump CABG regarding HITS and neurocognitive outcomes. Our findings confirm the association between cerebral microemboli and an impairment in postoperative cognitive tests. This supports the hypothesis that both microemboli and cognitive impairment are strongly related to CPB. With this in mind, the advantages of off-pump operations on neurocognitive outcome appear to be promising.
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Acknowledgments |
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Footnotes |
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S. Verma, P. W.M. Fedak, R. D. Weisel, P. E. Szmitko, M. V. Badiwala, D. Bonneau, D. Latter, L. Errett, and Y. LeClerc Off-Pump Coronary Artery Bypass Surgery: Fundamentals for the Clinical Cardiologist Circulation, March 16, 2004; 109(10): 1206 - 1211. [Full Text] [PDF]
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G. K. Peel, S. C. Stamou, M. K. C. Dullum, P. C. Hill, K. A. Jablonski, A. S. Bafi, S. W. Boyce, K. R. Petro, and P. J. Corso Chronologic distribution of stroke after minimally invasive versus conventional coronary artery bypass J. Am. Coll. Cardiol., March 3, 2004; 43(5): 752 - 756. [Abstract] [Full Text] [PDF]
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R. Motallebzadeh, R. Kanagasabay, M. Bland, J. C. Kaski, and M. Jahangiri S100 protein and its relation to cerebral microemboli in on-pump and off-pump coronary artery bypass surgery Eur. J. Cardiothorac. Surg., March 1, 2004; 25(3): 409 - 414. [Abstract] [Full Text] [PDF]
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P.-G. Chassot, P. van der Linden, M. Zaugg, X. M. Mueller, and D. R. Spahn Off-pump coronary artery bypass surgery: physiology and anaesthetic management{dagger} Br. J. Anaesth., March 1, 2004; 92(3): 400 - 413. [Abstract] [Full Text] [PDF]
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M. J. Racz, E. L. Hannan, O. W. Isom, V. A. Subramanian, R. H. Jones, J. P. Gold, T. J. Ryan, A. Hartman, A. T. Culliford, E. Bennett, et al. A comparison of short- and long-term outcomes after off-pump and on-pump coronary artery bypass graft surgery with sternotomy J. Am. Coll. Cardiol., February 18, 2004; 43(4): 557 - 564. [Abstract] [Full Text] [PDF]
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M. Pocar and F. Donatelli Abdominal tumors with cavoatrial extension J. Thorac. Cardiovasc. Surg., January 1, 2004; 127(1): 301 - 302. [Full Text] [PDF]
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H. K. Song, R. J. Petersen, E. Sharoni, R. A. Guyton, and J. D. Puskas Safe evolution towards routine off-pump coronary artery bypass: negotiating the learning curve Eur. J. Cardiothorac. Surg., December 1, 2003; 24(6): 947 - 952. [Abstract] [Full Text] [PDF]
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J. Wippermann, J. M. Albes, H. Brandes, H. Kosmehl, R. Bruhin, and T. Wahlers Acute effects of tourniquet occlusion and intraluminal shunts in beating heart surgery Eur. J. Cardiothorac. Surg., November 1, 2003; 24(5): 757 - 761. [Abstract] [Full Text] [PDF]
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P. Hughes, J.M. Hasenkam, I.K. Severinsen, and D.A. Steinbruchel Right heart assist for beating heart coronary artery bypass grafting Eur. J. Cardiothorac. Surg., November 1, 2003; 24(5): 762 - 769. [Abstract] [Full Text] [PDF]
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J. T. Reston, S. J. Tregear, and C. M. Turkelson Meta-analysis of short-term and mid-term outcomes following off-pump coronary artery bypass grafting Ann. Thorac. Surg., November 1, 2003; 76(5): 1510 - 1515. [Abstract] [Full Text] [PDF]
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J. E. Scarborough, W. White, F. E. Derilus, J. P. Mathew, M. F. Newman, and K. P. Landolfo Combined use of off-pump techniques and a sutureless proximal aortic anastomotic device reduces cerebral microemboli generation during coronary artery bypass grafting J. Thorac. Cardiovasc. Surg., November 1, 2003; 126(5): 1561 - 1567. [Abstract] [Full Text] [PDF]
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G. D'Ancona, J. I. S. de Ibarra, R. Baillot, P. Mathieu, D. Doyle, J. Metras, D. Desaulniers, and F. Dagenais Determinants of stroke after coronary artery bypass grafting Eur. J. Cardiothorac. Surg., October 1, 2003; 24(4): 552 - 556. [Abstract] [Full Text] [PDF]
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D. L. Ngaage Off-pump coronary artery bypass grafting: the myth, the logic and the science Eur. J. Cardiothorac. Surg., October 1, 2003; 24(4): 557 - 570. [Abstract] [Full Text] [PDF]
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C. Lund, P. K. Hol, R. Lundblad, E. Fosse, K. Sundet, B. Tennoe, R. Brucher, and D. Russell Comparison of cerebral embolization during off-pump and on-pump coronary artery bypass surgery Ann. Thorac. Surg., September 1, 2003; 76(3): 765 - 770. [Abstract] [Full Text] [PDF]
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M. Perthel, S. Kseibi, A. Bendisch, and J. Laas The dynamic bubble trap reduces microbubbles in extracorporeal circulation and high intensity transient signals in the middle cerebral artery: a case report Perfusion, September 1, 2003; 18(5): 325 - 329. [Abstract] [PDF]
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F. F. Immer, P. A. Berdat, A. S. Immer-Bansi, F. S. Eckstein, S. Muller, H. Saner, and T. P. Carrel Benefit to quality of life after Off-Pump versus On-Pump coronary bypass surgery Ann. Thorac. Surg., July 1, 2003; 76(1): 27 - 31. [Abstract] [Full Text] [PDF]
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A. Parolari, F. Alamanni, A. Cannata, M. Naliato, L. Bonati, P. Rubini, F. Veglia, E. Tremoli, and P. Biglioli Off-pump versus on-pump coronary artery bypass: meta-analysis of currently available randomized trials Ann. Thorac. Surg., July 1, 2003; 76(1): 37 - 40. [Abstract] [Full Text] [PDF]
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D. J. Goldstein, R. B. Beauford, B. Luk, R. Karanam, T. Prendergast, F. Sardari, P. Burns, and C. Saunders Multivessel off-pump revascularization in patients with severe left ventricular dysfunction Eur. J. Cardiothorac. Surg., July 1, 2003; 24(1): 72 - 80. [Abstract] [Full Text] [PDF]
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T. Goto, T. Baba, K. Matsuyama, K. Honma, M. Ura, and T. Koshiji Aortic atherosclerosis and postoperative neurological dysfunction in elderly coronary surgical patients Ann. Thorac. Surg., June 1, 2003; 75(6): 1912 - 1918. [Abstract] [Full Text] [PDF]
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R. Ascione and G. D. Angelini Off-pump coronary artery bypass surgery: The implications of the evidence J. Thorac. Cardiovasc. Surg., April 1, 2003; 125(4): 779 - 781. [Full Text] [PDF]
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A. M.A. Keizer, R. Hijman, D. van Dijk, C. J. Kalkman, and R. S. Kahn Cognitive self-assessment one year after on-pump and off-pump coronary artery bypass grafting Ann. Thorac. Surg., March 1, 2003; 75(3): 835 - 838. [Abstract] [Full Text] [PDF]
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J. Bucerius, J. F. Gummert, M. A. Borger, T. Walther, N. Doll, J. F. Onnasch, S. Metz, V. Falk, and F. W. Mohr Stroke after cardiac surgery: a risk factor analysis of 16,184 consecutive adult patients Ann. Thorac. Surg., February 1, 2003; 75(2): 472 - 478. [Abstract] [Full Text] [PDF]
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R Ascione and G.D Angelini OPCAB surgery: a voyage of discovery back to the future Eur. Heart J., January 2, 2003; 24(2): 121 - 124. [Full Text] [PDF]
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A. Mazzone, J. Gianetti, E. Picano, S. Bevilacqua, G. Zucchelli, A. Biagini, and M. Glauber Correlation between inflammatory response and markers of neuronal damage in coronary revascularization with and without cardiopulmonary bypass Perfusion, January 1, 2003; 18(1): 3 - 8. [Abstract] [PDF]
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A. G. Cerillo, L. Sabatino, S. Bevilacqua, P. A. Farneti, M. Scarlattini, F. Forini, and M. Glauber Nonthyroidal illness syndrome in off-pump coronary artery bypass grafting Ann. Thorac. Surg., January 1, 2003; 75(1): 82 - 87. [Abstract] [Full Text] [PDF]
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J. Laas, S. Kseibi, M. Perthel, A. Klingbeil, L'E. El-Ayoubi, and A. Alken Impact of high intensity transient signals on the choice of mechanical aortic valve substitutes Eur. J. Cardiothorac. Surg., January 1, 2003; 23(1): 93 - 96. [Abstract] [Full Text] [PDF]
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R. Ascione, M. Caputo, and G. D. Angelini Off-pump coronary artery bypass grafting: not a flash in the pan Ann. Thorac. Surg., January 1, 2003; 75(1): 306 - 313. [Abstract] [Full Text] [PDF]
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V. Pignay-Demaria, F. Lesperance, R. G. Demaria, N. Frasure-Smith, and L. P. Perrault Depression and anxiety and outcomes of coronary artery bypass surgery Ann. Thorac. Surg., January 1, 2003; 75(1): 314 - 321. [Abstract] [Full Text] [PDF]
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J. W. Hammon Jr. and L. H. Edmunds Jr. Extracorporeal Circulation: Organ Damage Card. Surg. Adult, January 1, 2003; 2(2003): 361 - 388. [Full Text]
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R. Salenger, J. S. Gammie, and T. J. Vander Salm Postoperative Care of Cardiac Surgical Patients Card. Surg. Adult, January 1, 2003; 2(2003): 439 - 469. [Full Text]
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V. Vijay and J. P. Gold Late Complications of Cardiac Surgery Card. Surg. Adult, January 1, 2003; 2(2003): 521 - 537. [Full Text]
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T. M. Dewey and M. J. Mack Myocardial Revascularization Without Cardiopulmonary Bypass Card. Surg. Adult, January 1, 2003; 2(2003): 609 - 625. [Full Text]
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C. S. Hollenbeak, D. L. Morris, and M. C. Sinclair Is Off-pump Coronary Artery Bypass Graft Surgery Cost-Saving? Seminars in Cardiothoracic and Vascular Anesthesia, December 1, 2002; 6(4): 325 - 329. [Abstract] [PDF]
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V. Zamvar, D. Williams, J. Hall, N. Payne, C. Cann, K. Young, S Karthikeyan, and J. Dunne Assessment of neurocognitive impairment after off-pump and on-pump techniques for coronary artery bypass graft surgery: prospective randomised controlled trial BMJ, November 30, 2002; 325(7375): 1268 - 1268. [Abstract] [Full Text] [PDF]
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K.-B. Kim, C. H. Kang, W.-I. Chang, C. Lim, J. H. Kim, B. M. Ham, and Y. L. Kim Off-pump coronary artery bypass with complete avoidance of aortic manipulation Ann. Thorac. Surg., October 1, 2002; 74(4): S1377 - 1382. [Abstract] [Full Text] [PDF]
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M. Mack, D. Bachand, T. Acuff, J. Edgerton, S. Prince, T. Dewey, and M. Magee Improved outcomes in coronary artery bypass grafting with beating-heart techniques J. Thorac. Cardiovasc. Surg., September 1, 2002; 124(3): 598 - 607. [Abstract] [Full Text] [PDF]
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 A. Diegeler, H. Thiele, V. Falk, R. Hambrecht, N. Spyrantis, P. Sick, K. W. Diederich, F. W. Mohr, and G. Schuler Comparison of Stenting with Minimally Invasive Bypass Surgery for Stenosis of the Left Anterior Descending Coronary Artery N. Engl. J. Med., August 22, 2002; 347(8): 561 - 566. [Abstract] [Full Text] [PDF]
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S. C. Stamou, K. A. Jablonski, A. J. Pfister, P. C. Hill, M. K.C. Dullum, A. S. Bafi, S. W. Boyce, K. R. Petro, and P. J. Corso Stroke after conventional versus minimally invasive coronary artery bypass Ann. Thorac. Surg., August 1, 2002; 74(2): 394 - 399. [Abstract] [Full Text] [PDF]
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N.C. Patel, A.D. Grayson, M. Jackson, J. Au, N. Yonan, R. Hasan, and B.M. Fabri The effect off-pump coronary artery bypass surgery on in-hospital mortality and morbidity Eur. J. Cardiothorac. Surg., August 1, 2002; 22(2): 255 - 260. [Abstract] [Full Text] [PDF]
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R. Ascione, S. Al-Ruzzeh, K. Amer, and G. D Angelini Subsystem organ function during coronary surgery Perfusion, July 1, 2002; 17(4): 295 - 303. [Abstract] [PDF]
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F. M. Fouad-Tarazi, J. Feldschuh, S. M. F. Malheiros, A. R. Massaro, E. Buffolo, D. Venes, W. T. C. Yuh, C. J. Knott-Craig, M. D. Tilak, D. van Dijk, et al. Cognitive Outcomes Following Cardiopulmonary Bypass JAMA, June 19, 2002; 287(23): 3077 - 3079. [Full Text] [PDF]
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E. W. Jansen Invited Commentary Asian Cardiovasc Thorac Ann, June 1, 2002; 10(2): 158 - 159. [Full Text] [PDF]
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D. Van Dijk, E. W. L. Jansen, R. Hijman, A. P. Nierich, J. C. Diephuis, K. G. M. Moons, J. R. Lahpor, C. Borst, A. M. A. Keizer, H. M. Nathoe, et al. Cognitive Outcome After Off-Pump and On-Pump Coronary Artery Bypass Graft Surgery: A Randomized Trial JAMA, March 20, 2002; 287(11): 1405 - 1412. [Abstract] [Full Text] [PDF]
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D. B. Mark and M. F. Newman Protecting the Brain in Coronary Artery Bypass Graft Surgery JAMA, March 20, 2002; 287(11): 1448 - 1450. [Full Text] [PDF]
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H. L. Karamanoukian, H. W. Donias, and J. Bergsland Decreased incidence of postoperative stroke following off-pump coronary artery bypass J. Am. Coll. Cardiol., March 6, 2002; 39(5): 917 - 917. [Full Text] [PDF]
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D C Whitaker, J Stygall, and S P Newman Neuroprotection during cardiac surgery: strategies to reduce cognitive decline Perfusion, March 1, 2002; 17(2_suppl): 69 - 75. [Abstract] [PDF]
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O. Chavanon, M. Durand, R. Hacini, H. Bouvaist, M. Noirclerc, T. Ayad, and D. Blin Coronary artery bypass grafting with left internal mammary artery and right gastroepiploic artery, with and without bypass Ann. Thorac. Surg., February 1, 2002; 73(2): 499 - 504. [Abstract] [Full Text] [PDF]
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