HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): William R. Brown John W. Hammon, Jr David A. Stump Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Brooker, R. F. Articles by Stump, D. A. Search for Related Content PubMed PubMed Citation Articles by Brooker, R. F. Articles by Stump, D. A.

Ann Thorac Surg 1998;65:1651-1655
© 1998 The Society of Thoracic Surgeons

---

Original articles: cardiovascular

Cardiotomy Suction: A Major Source of Brain Lipid Emboli During Cardiopulmonary Bypass

^a Department of Anesthesia, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA
^b Department of Radiology, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA
^c the Program in Neuroscience, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA
^d Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA
^e Department of Cardiothoracic Surgery, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA
^f Department of Public Health Sciences, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA

Accepted for publication January 29, 1998.

Address reprint requests to Dr Moody, Department of Radiology, Wake Forest University School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157-1088
e-mail: (moodyd{at}radmin.rad.bgsm.edu)

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. Brain injury remains a significant problem in patients undergoing cardiac surgery assisted by cardiopulmonary bypass (CPB). Autopsy brain specimens of patients after cardiac operations with CPB reveal numerous acellular lipid deposits (10 to 70 µm) in the microvasculature. We hypothesize that these small capillary and arterial dilatations result from a diffuse inflammatory response to CPB or from emboli delivered by the bypass circuit. This study was undertaken to determine which aspect of CPB is most clearly associated with these dilatations.

Methods. Thirteen dogs were studied in four groups: group I (n = 3), right-heart CPB; group II (n = 2), lower-extremity CPB; group III (n = 3), hypothermic CPB; and group IV (n = 5), hypothermic CPB with cardiotomy suction. All dogs in all groups were maintained on CPB for 60 minutes and then euthanized. Brain specimens were harvested, fixed in ethanol, embedded in celloidin, and stained with the alkaline phosphate histochemical technique so that dilatations could be counted.

Results. All dogs completed the protocol. The mean density of dilatations per square centimeter for each group was as follows: group I, 1.77 ± 0.77; group II, 4.17 ± 1.65; group III, 4.54 ± 1.69; and group IV, 46.5 ± 14.5. In group IV (cardiotomy suction), dilatation density was significantly higher than in group III (hypothermic cardiopulmonary bypass) (p = 0.04) and all other groups (p = 0.04).

Conclusions. Blood aspirated from the surgical field and subsequently reinfused into dogs undergoing CPB produces a greater density of small capillary and arterial dilatations than CPB without cardiotomy suction, presumably because of lipid microembolization.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Despite continual improvements in surgical technique and cardiopulmonary bypass (CPB) equipment, postoperative neurologic deterioration remains a frequent problem in patients undergoing cardiac operations [1]. The cause of brain injury during cardiac operations is almost certainly multifactorial, but mounting evidence suggests that microemboli play an important role. Examination of cerebral spinal fluid and blood has identified elevated enzymatic protein markers of brain injury in 6% to 50% of patients undergoing cardiac operations [2–4]. Moreover, neuropsychological deterioration in these patients is correlated with increases in cerebral spinal fluid markers of brain injury. Evidence linking microemboli to neurologic complications is supported by studies using carotid and transcranial Doppler ultrasound [5–7] during CPB and by examinations of retinal microvascular occlusions [8] during and after CPB. Many sources of microemboli during open heart surgery have been suggested in the literature, including dislodgement of atheromatous debris from the aorta, release of left-ventricular thrombus, and microembolism of air, fat, platelet aggregates, fiber, or silicone [9, 10]. Moody and colleagues [11] first documented the presence of small capillary and arterial dilatations (SCADs) in autopsy specimens from patients who had undergone cardiac operations assisted by CPB. These SCADs appear to result from emboli and can be found in other organs as well as the brain [12]. Small capillary and arterial dilatations are not encountered unless the patient or experimental animal has undergone a recent interarterial intervention proximal (with respect to the circulation pathway) to the organ being examined [13]. Although the exact cause of SCADs remains unknown, evidence suggests that lipid microemboli may play an important role in SCAD formation [14, 15]. In experimental preparations, the presence of SCADs in the brain is associated with evidence of localized tissue injury [12]. The embolic material responsible for the SCAD phenomenon is largely removed by the solvents used in tissue processing, so SCADs represent the footprint of the emboli as seen on alkaline phosphatase histochemical microvascular staining. We have performed elemental analysis on the residue of this exogenous material with laser microprobe mass spectrometry. Aluminum and silicon are found in increased concentrations in the SCADs and surrounding brain parenchyma [16]. Controlling for length of postoperative patient survival, the SCAD density in brain tissue is proportional to the duration of bypass (Brown WR et al, unpublished results). In addition, we have demonstrated brain tissue injury in the vicinity of SCADs manifested by focal vacuolation, neuronal loss, and swollen astrocytic end-feet [13].

In the present investigation, we sought to determine if SCADs are caused by an inflammatory response to CPB, or are caused by microemboli from the CPB circuit. To determine which aspect of CPB is most clearly associated with SCADs, we examined the brains of dogs in four groups subjected to CPB wherein cannulation site, temperature, and use of cardiotomy suction were varied.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Subject groups
Thirteen dogs weighing 24.5 to 30 kg each were studied in four groups with varied CPB protocols. All dogs were adult, mongrel animals between the ages of 1 and 2 years. These dogs were obtained through the Animal Resource Center from a United States Department of Agriculture-licensed vendor. All dogs received humane treatment in accordance with the "Guide for the Care and Use of Laboratory Animals" prepared by the Institute of Laboratory Animal Resources and published by the National Institutes of Health (NIH publication 86-23, revised 1985).

Dogs in group I underwent right-heart CPB. Arterial inflow from CPB was infused into the pulmonary artery, and systemic perfusion was maintained with the native circulation. Venous drainage was accomplished through bicaval right-atrial cannulation. Minimum CPB flow was maintained at 100 mL/kg per minute, with a minimum mean arterial pressure (MAP) of 40 mm Hg and a temperature of 37°C.

Dogs in group II underwent lower-extremity CPB. The arterial cannula was placed in the left femoral artery to perfuse the lower extremities, and venous cannulas were placed in the right atrium. At the start of CPB, the descending thoracic aorta was clamped at the diaphragm, and approximately 50% of venous return was diverted to the CPB pump. The remaining venous return was pumped through the heart to the lungs, head, and front legs. Cardiopulmonary bypass flow was maintained at 50 to 70 mL/kg per minute, with a minimum MAP of 40 mm Hg and a temperature of 37°C.

In group III, hypothermic CPB was accomplished through an arterial inflow cannula in the transverse aorta (placed through the left subclavian artery) with venous return through bicaval right-atrial cannulation. Minimum CPB flow at normothermia was 100 mL/kg per minute and 50 mL/kg per minute at hypothermia (25°C), with a minimum MAP of 40 mm Hg.

In group IV, hypothermic CPB with cardiotomy suction, CPB was accomplished in the same manner as in group III, but cardiotomy suction was used to evacuate shed blood from the operative field and subsequently filtered and variably reinfused into the dog during CPB. Bleeding into the operative field was promoted by lacerating intercostal arteries. This maneuver was not used in the other groups. The volume of cardiotomy suction varied for dogs in group IV.

For dogs in groups III and IV, normothermia lasted for 10 minutes before cooling and 10 minutes at the conclusion of cold CPB. Cooling and rewarming periods were 10 minutes each and hypothermic CPB lasted for 20 minutes.

In all dogs, pH was maintained between 7.4 and 7.5, carbon dioxide tension was maintained at 30 to 45 mm Hg, and arterial oxygen tension between 150 and 200 mm Hg throughout the experiment. Activated clotting time was greater than 400 seconds during the CPB period, and CPB duration was 60 minutes for all dogs. To maintain minimum MAP in all dog groups, a phenylephrine infusion at 60 µg/mL was started when MAP decreased to less than 40 mm Hg and was titrated to maintain this minimum MAP during the CPB time.

Cardiopulmonary bypass circuit
Cardiopulmonary bypass was conducted by means of an adult circuit containing the following: from Bently (Irvine, CA), 3/8-inch arterial tubing, -inch venous tubing, and -inch suction tubing, cardiotomy reservoir (model BCR-3500 with polyester tricot filter sock, 150 to 200 µm pore size), heparin-coated venous reservoir (model P107386-01), and arterial filter (model AF-1025) (25 µm); from 3M Health Care Sarns (Ann Arbor, MI), membrane oxygenator (model 9443), Heater/Cooler Unit, and roller pump (model 5000). All disposable components of the CPB apparatus were from the same manufacturer and lot number. The CPB circuit was purged with CO₂ and primed with 1,000 mL of lactated Ringer’s solution, 25 g of mannitol, 250 mL of 5% albumin, 50 mEq of sodium bicarbonate, and 5,000 units of heparin. After priming, the entire bypass circuit, including the cardiotomy suction reservoir, was allowed to circulate intact to promote optimal removal of air. Nasopharyngeal and aortic inflow blood temperatures were recorded every 5 minutes during CPB. Mean arterial pressure and pump flow rates were recorded every 10 minutes during CPB. We managed PCO₂ and pH by using an -stat strategy. All dogs were placed on identically prepared CPB circuits, which all contained the cardiotomy reservoir.

Animal preparation
When a dog arrived in the laboratory, an intravenous catheter (glucose-free, lactated Ringer’s solution) was placed in its right or left front leg. Anesthesia was induced by administration of thiopental sodium 500 mg with a bolus of fentanyl 200 µg/kg and diazepam 1 mg/kg. Anesthesia was maintained with an infusion of fentanyl and diazepam (0.8 µg/kg per minute and 1.0 µg/kg per minute, respectively). The dogs were placed in supine position, and a Bovie pad was applied to a foreleg. Femoral arterial and venous lines were placed. The hair along the anterior aspect of the sternum was shaved, and a midline incision was made from the level of the sternal notch to the xyphoid process. The thorax was opened with an oscillating sternal saw followed by placement of rib spreaders and application of bone wax to limit blood loss from bone marrow. The superior and inferior vena cava were identified and umbilical tapes placed around these structures. Heparin was administered at 300 U/kg, and an activated clotting time greater than 400 seconds was obtained. For dogs in groups III and IV, a 20F aortic inflow cannula (Bard, Santa Ana, CA) was placed through the left subclavian artery to the level of the transverse aortic arch. For dogs in group I, a 20F inflow cannula was positioned in the main pulmonary artery through a right ventriculotomy incision. In group II dogs, a 20F inflow cannula was placed in the left femoral artery. In all dogs, bicaval venous cannulation with 28F single-stage cannulas (Bard) was performed through a right atriotomy incision. In group IV animals, the electrocautery was used to make several linear cuts along the anterior inner aspect of the chest wall. In doing so, blood vessels, fat, and muscle tissue were lacerated, and the resulting blood and tissue fluid was allowed to drain into the pericardial well where it was aspirated using a cardiotomy suction catheter (Yankauer, model 298). This maneuver was performed to simulate the dissection around the heart and great vessels that accompanies clinical cardiac operations.

No additional blood was given to dogs in groups I and III. Blood aspirated into the cardiotomy suction was replaced with lactated Ringer’s solution and not returned to the CPB pump. The average cardiotomy suction volume in groups I and III was less than 150 mL.

Hematocrits varied between dogs at baseline and accordingly on CPB with hemodilution from the CPB prime. We did not transfuse dogs with additional blood, to eliminate this as a potential source of SCADs. No specific target hematocrit was maintained during the perioperative period.

The CPB pump was assembled in an identical fashion to assembly of circuits for human use in our main operating room. The arterial filter was located in standard position on the arterial inflow line distal to the oxygenator. The circuit was primed with 5,000 U heparin for all dogs.

SCAD density determination
After 60 minutes of CPB, dogs were euthanized with an injection of potassium chloride. The brains were immediately removed and fixed in cold 70% ethanol. A 1.5-cm-thick coronal whole-brain slice just posterior to the foramen of Monro was processed through graded alcohols and ether before being embedded in celloidin. The celloidin block was serially sectioned at a thickness of 100 µm to obtain ten sections. The sections were serially numbered and stained with Bell and Scarrow’s [17] modification of the Gomori method for alkaline phosphatase histochemistry, which results in the precipitation of black lead sulfide at sites reactive for alkaline phosphatase, in this case endothelial cells lining the afferent microvessels. Coronal sections of the entire brain, 100 µm thick and encompassing both left and right hemispheres attached by the corpus callosum, were stained with alkaline phosphatase, mounted on large glass slides, and coverslipped. For counting SCADs, a standardized area was established on the slide. With a permanent, extrafine marker pen, the perimeter of a standardized area in the left hemisphere was drawn. This standardized area typically encompassed the cingulate, lateral, suprasylvian, and medial ectosylvian gyri. The white matter component of such an area consisted of subcortical white matter and radiation of corpus callosum down to the level of the supralateral angle of the lateral ventricle. The standardized area contained an approximately equal ratio of cortical gray and white matter tissue. Subsequently, the dimension of the surface of such an area was quantified with a computerized planar morphometry image analysis system (NIH image with a Scion LG3 card). Typically, the surface of the standardized area was approximately 1.2 cm². Small capillary and arterial dilatations in this clearly demarcated area were then counted by a blinded observer (H.S.G.-B.) in a systematic manner in one microscopic field at a time, with a 10x objective, focusing up and down through the thickness of the section (Fig 1).

View larger version (101K): [in this window] [in a new window]   Fig 1. Small capillary and arterial dilatations (SCADs) (arrows) in cerebral vessels in a dog after cardiopulmonary bypass with cardiotomy suction. (Alkaline phosphatase-stained celloidin section, 100 µm thick; x25 before 50% reduction.)

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
All dogs completed the protocol. Density of SCADs and cardiotomy suction volume (group IV) for each dog are shown in Table 1. The mean SCAD density per square centimeter in each group was as follows: group I, 1.77 ± 0.77; group II, 4.17 ± 1.65; group III, 4.54 ± 1.69; and group IV, 46.5 ± 14.5. The mean SCAD density for each group is shown in Figure 2. There was a markedly larger variance in group IV than in group III; this difference was statistically significant (F = 122, p = 0.016).

View larger version (14K): [in this window] [in a new window]   Fig 2. Small capillary and arterial dilatation (SCAD) counts for dogs by group: group I = right-heart cardiopulmonary bypass (CPB), group II = lower extremity CPB, group III = hypothermic CPB, and group IV = hypothermic CPB with cardiotomy suction. Dots denote individual dogs, and lines represent the mean for each group. Mean and standard error of the mean for each group are given at the top of the figure.

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
In the present study, we sought to determine if SCADs are caused by emboli delivered from the CPB circuit or are caused by an inflammatory response to the CPB circuit. The most notable finding of this study is that dogs exposed to CPB with cardiotomy suction (group IV) exhibited significantly more SCADs than dogs in all other groups (46.5 ± 14.5 versus 3.41 ± 0.83 SCADs per cm²; p = 0.04). Further, dogs in group IV (hypothermic CPB with cardiotomy suction) had significantly more SCADs than dogs in group III (hypothermic CPB) (46.5 ± 14.5 versus 4.54 ± 1.7 SCADs per cm²; p = 0.04). This suggests that cardiotomy suction blood may be the most important source of lipid emboli and SCAD density. Solis and associates [19] noted that cardiotomy suction was a major source of microemboli, as measured with a Coulter counter in samples from the cardiotomy reservoir line and other sites. Microemboli were most numerous during periods of vigorous cardiotomy suction [19]. These observations have been confirmed recently with more modern bypass equipment by Liu and colleagues [20], who demonstrated high numbers of microemboli from cardiotomy suction, again using the Coulter counter [20]. Our experiment shows a direct relationship between cardiotomy suction and the number of cerebral SCADs. This relationship strongly suggests that a substantial portion of microemboli results from blood reinfused through the CPB circuit and that current venous and arterial filters inadequately protect patients from lipid microemboli.

The number of SCADs in the cardiotomy suction group did not correlate with the volume of cardiotomy suction. We believe the lack of correlation between cardiotomy suction volume and SCAD density is a result of not controlling the conditions of cardiotomy suction. In some dogs, there was more tissue and pericardial fat disruption leading to larger amounts of lipid in the cardiotomy suction blood. A larger lipid emboli load could result in greater SCAD density, independent of cardiotomy blood volume. Dogs in which the cardiotomy suction volume was primarily caused by bleeding from arterial and venous cannulation sites (blood with potentially lower amounts of disrupted lipid and tissue debris) would have greater cardiotomy suction volumes, but low SCAD density. Finally, we did not standardize the time during which the cardiotomy suction was aspirated from the operative field relative to cooling and warming on CPB. Cardiotomy suction during hypothermic CPB compared to normothermic CPB could result in fewer SCADs because of the lower net cerebral blood flow at hypothermic temperatures.

We also sought to determine if the lung could act as a natural filter and reduce SCAD density. In groups I and II, blood first passed through the lungs before perfusing the dog brain. We hoped to detect any filtering effect of emboli by the lung in these groups compared to group III (hypothermic CPB). There was no statistically significant difference in SCAD density between groups I, II, and III. However, the number of dogs in groups I, II, and III is small, making comparisons between these groups difficult. In addition, maintaining heart function in groups I and II required that normothermia be maintained and further complicated comparison with group III, which underwent hypothermic CPB. We noted that SCAD density was lower in groups I, II, and III than previously detected in other studies, which used a bubble oxygenator rather than a membrane oxygenator [11–13, 15]. Therefore, we are unable to determine whether the lung can effectively reduce SCAD density.

As mentioned previously, we have observed a correlation in human patients undergoing cardiac operations between the duration of CPB and cerebral SCAD density. In the present experiment we did not attempt to correlate duration of CPB and cerebral SCAD density, as all dogs underwent an equal duration of CPB.

An additional aim of this study was to determine if SCADs are a result of an inflammatory process associated with CPB. Dogs in group II underwent CPB support of the lower extremities only; blood flow to the brain and upper body was sustained entirely by the native circulation. In this group no emboli could be delivered directly to the brain through the CPB circuit. Therefore, if SCADs appeared in the brain, they could potentially be attributed to an inflammatory response, insudation of lipid into the vessels from the surrounding brain parenchyma during fixation, or emboli passing through the lungs and lodging secondarily in the afferent brain microvessels. We did not find a significant difference in SCAD density between groups I, II, and III, suggesting little role for inflammation. However, because all three groups were exposed to CPB, we are unable to exclude an inflammatory process as a cause for the low number of SCADs observed.

There are a number of limitations to this study. We did not measure the amount or type of lipid in the cardiotomy bloodstream. As described above, knowledge of the concentration and total lipid content contained in the cardiotomy blood would help strengthen the association between lipid embolization and SCAD density. We did not specifically measure markers of inflammation in each dog group. Measurement of inflammatory mediators would be helpful in understanding the role of inflammation and SCADs. The number of dogs in each group was small, and the numbers differed between groups. This was because of the limited availability of CPB circuits from the same manufacturer’s lot number, and that marked statistical significance was observed with group IV animals. Finally, dogs were not randomly assigned to each of the four groups tested.

In conclusion, this study demonstrates that the aspiration of shed blood from the surgical field, followed by reinfusion through the CPB pump, results in a marked increase in the number of SCADs. Given that SCADs may reflect lipid emboli to the microcirculation of the brain, our data suggest that a major source of these emboli is the suctioning of blood from the surgical field. In addition, the 25-µm arterial line filters currently used do not adequately remove these emboli from the CPB circuit. More effective means to filter or process blood aspirated from the surgical field and returned to the patient through the cardiopulmonary bypass circuit appear warranted.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
We acknowledge Shirley Blakemore and Pat Wood for preparation of the histologic specimens, Jason Vernon for assistance with the CPB apparatus, and Donna S. Garrison, PhD, and Terry R. Poovey for expert editing of the manuscript.

This study was supported by National Institutes of Health grants NS20618 and NS275000.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

1. Rogers A.T., Neuman S.P., Stump D.A., Prough D.S. Neurologic effects of cardiopulmonary bypass. In: Gravlee G.P., Davis R.F., Utley J.R., eds. Cardiopulmonary bypass: principles and practice. Baltimore: Williams & Wilkins, 1993:542-576.
2. Aberg T., Ronquist G., Tyden H., et al. Adverse effects on the brain in cardiac operations as assessed by biochemical, psychometric, and radiologic methods. J Thorac Cardiovasc Surg 1984;87:99-105.[Abstract]
3. Steinberg G.K., De La Paz R., Mitchell R.S., Bell T.E., Albers G.W. MR and cerebrospinal fluid enzymes as sensitive indicators of subclinical cerebral injury after open-heart valve replacement surgery. AJNR Am J Neuroradiol 1996;17:205-212.[Abstract]
4. Johnsson P. Markers of cerebral ischemia after cardiac surgery. J Cardiothorac Vasc Anesth 1996;10:120-126.[Medline]
5. Padayachee T.S., Parsons S., Theobold R., Linley J., Gosling R.G., Deverall P.B. The detection of microemboli in the middle cerebral artery during cardiopulmonary bypass: a transcranial Doppler ultrasound investigation using membrane and bubble oxygenators. Ann Thorac Surg 1987;44:298-302.[Abstract]
6. Stump D.A., Kon N.A., Rogers A.T., Hammon J.W. Emboli and neuropsychological outcome following cardiopulmonary bypass. Echocardiography 1996;13:555-558.[Medline]
7. Van der Linden J., Casimir-Ahn H. When do cerebral emboli appear during open heart operations? A transcranial Doppler study. Ann Thorac Surg 1991;51:237-241.[Abstract]
8. Blauth C.I., Arnold J.V., Schulenberg W.E., McCartney A.C., Taylor K.M. Cerebral microembolism during cardiopulmonary bypass. Retinal microvascular studies in vivo with fluorescein angiography. J Thorac Cardiovasc Surg 1988;95:668-676.[Abstract]
9. Slogoff S., Girgis K.Z., Keats A.S. Etiologic factors in neuropsychiatric complications associated with cardiopulmonary bypass. Anesth Analg 1982;61:903-911.[Abstract/Free Full Text]
10. Shaw P.J., Bates D., Cartlidge N.E., Heaviside D., Julian D.G., Shaw D.A. Early neurological complications of coronary artery bypass surgery. Br Med J 1985;291:1384-1387.
11. Moody D.M., Bell M.A., Challa V.R., Johnston W.E., Prough D.S. Brain microemboli during cardiac surgery or aortography. Ann Neurol 1990;28:477-486.[Medline]
12. Challa V.R., Moody D.M., Troost B.T. Brain embolic phenomena associated with cardiopulmonary bypass. J Neurol Sci 1993;117:224-231.[Medline]
13. Moody D.M., Brown W.R., Challa V.R., Stump D.A., Reboussin D.M., Legault C. Brain microemboli associated with cardiopulmonary bypass: a histologic and magnetic resonance imaging study. Ann Thorac Surg 1995;59:1304-1307.[Abstract/Free Full Text]
14. Brown W.R., Moody D.M., Stump D.A., Deal D.D., Anderson R.L. Dog model for cerebrovascular studies of the proximal-to-distal distribution of sequentially injected emboli. Microvasc Res 1995;50:105-112.[Medline]
15. Brown W.R., Moody D.M., Challa V.R., Stump D.A. Histologic studies of brain microemboli in humans and dogs after cardiopulmonary bypass. Echocardiography 1996;13:559-565.[Medline]
16. Challa V.R., Lovell M.A., Moody D.M., Brown W.R., Reboussin D.M., Markesbery W.R. Laser microprobe mass spectrometric study of aluminum and silicon in brain emboli related to cardiac surgery. J Neuropathol Exp Neurol 1998;57:140-147.[Medline]
17. Bell M.A., Scarrow W.G. Staining for microvascular alkaline phosphatase in thick celloidin sections of nervous tissue: morphometric and pathological applications. Microvasc Res 1984;27:189-203.[Medline]
18. Snedecor G.W., Cochran W.G. Statistical methods, 7th ed. Ames, IA: Iowa State University Press, 1980:96-99.
19. Solis R.T., Noon G.P., Beall A.C., Jr, DeBakey M.E. Particulate microembolism during cardiac operation. Ann Thorac Surg 1974;17:332-344.[Medline]
20. Liu J.-F., Su Z.-K., Ding W.-X. Quantitation of particulate microemboli during cardiopulmonary bypass: experimental and clinical studies. Ann Thorac Surg 1992;54:1196-1202.[Abstract]

This article has been cited by other articles:

				A. Eyjolfsson, S. Scicluna, P. Johnsson, F. Petersson, and H. Jonsson Characterization of Lipid Particles in Shed Mediastinal Blood Ann. Thorac. Surg., March 1, 2008; 85(3): 978 - 981. [Abstract] [Full Text] [PDF]

				J. W. Hammon Extracorporeal Circulation: Perfusion System Card. Surg. Adult, January 1, 2008; 3(2008): 350 - 370. [Full Text]

				J. W. Hammon Extracorporeal Circulation: Organ Damage Card. Surg. Adult, January 1, 2008; 3(2008): 389 - 414. [Full Text]

				G. Djaiani, L. Fedorko, M. A. Borger, R. Green, J. Carroll, M. Marcon, and J. Karski Continuous-Flow Cell Saver Reduces Cognitive Decline in Elderly Patients After Coronary Bypass Surgery Circulation, October 23, 2007; 116(17): 1888 - 1895. [Abstract] [Full Text] [PDF]

				F. D. Rubens, M. Boodhwani, T. Mesana, D. Wozny, G. Wells, H. J. Nathan, and on behalf of the Cardiotomy Investigators The Cardiotomy Trial: A Randomized, Double-Blind Study to Assess the Effect of Processing of Shed Blood During Cardiopulmonary Bypass on Transfusion and Neurocognitive Function Circulation, September 11, 2007; 116(11_suppl): I-89 - I-97. [Abstract] [Full Text] [PDF]

				M. Appelblad and K. G. Engstrom Fat content in pericardial suction blood and the efficacy of spontaneous density separation and surface adsorption in a prototype system for fat reduction J. Thorac. Cardiovasc. Surg., August 1, 2007; 134(2): 366 - 372. [Abstract] [Full Text] [PDF]

				F. D. Rubens and H. Nathan Lessons learned on the path to a healthier brain: dispelling the myths and challenging the hypotheses Perfusion, May 1, 2007; 22(3): 153 - 160. [Abstract] [PDF]

				The Society of Thoracic Surgeons Blood Conservatio, V. A. Ferraris, S. P. Ferraris, S. P. Saha, E. A. Hessel II, C. K. Haan, B. D. Royston, C. R. Bridges, R. S.D. Higgins, G. Despotis, et al. Perioperative Blood Transfusion and Blood Conservation in Cardiac Surgery: The Society of Thoracic Surgeons and The Society of Cardiovascular Anesthesiologists Clinical Practice Guideline Ann. Thorac. Surg., May 1, 2007; 83(5_Supplement): S27 - S86. [Abstract] [Full Text] [PDF]

				M. Selim Perioperative Stroke N. Engl. J. Med., February 15, 2007; 356(7): 706 - 713. [Full Text] [PDF]

				P. D Raymond, M. Radel, M. J Ray, A. D Hinton-Bayre, and N. A Marsh Investigation of factors relating to neuropsychological change following cardiac surgery Perfusion, January 1, 2007; 22(1): 27 - 33. [Abstract] [PDF]

				K. J Lilly, J. M Balaguer, P. A Pirundini, M. A Smith, G. Connelly, L. J. Campbell, P. C Philie, M. McAdams, W. Riley, R. Dekkers, et al. Early results of a comprehensive operative and perfusion strategy to attenuate the incidence of adverse neurological outcomes in on-pump coronary artery bypass grafting (CABG) patients Perfusion, November 1, 2006; 21(6): 311 - 317. [Abstract] [PDF]

				Y. Abu-Omar, S. Cader, L. G. Wolf, D. Pigott, P. M. Matthews, and D. P. Taggart Short-term changes in cerebral activity in on-pump and off-pump cardiac surgery defined by functional magnetic resonance imaging and their relationship to microembolization. J. Thorac. Cardiovasc. Surg., November 1, 2006; 132(5): 1119 - 1125. [Abstract] [Full Text] [PDF]

				R. A Rodriguez and D. Belway Comparison of two different extracorporeal circuits on cerebral embolization during cardiopulmonary bypass in children Perfusion, September 1, 2006; 21(5): 247 - 253. [Abstract] [PDF]

				K. G. Shann, D. S. Likosky, J. M. Murkin, R. A. Baker, Y. R. Baribeau, G. R. DeFoe, T. A. Dickinson, T. J. Gardner, H. P. Grocott, G. T. O'Connor, et al. An evidence-based review of the practice of cardiopulmonary bypass in adults: A focus on neurologic injury, glycemic control, hemodilution, and the inflammatory response. J. Thorac. Cardiovasc. Surg., August 1, 2006; 132(2): 283 - 290.e3. [Full Text] [PDF]

				M. Carrier, A. Denault, J. Lavoie, and L. P. Perrault Randomized controlled trial of pericardial blood processing with a cell-saving device on neurologic markers in elderly patients undergoing coronary artery bypass graft surgery. Ann. Thorac. Surg., July 1, 2006; 82(1): 51 - 55. [Abstract] [Full Text] [PDF]

				J. M Murkin Pathophysiological Basis of CNS Injury in Cardiac Surgical Patients: Detection and Prevention Perfusion, July 1, 2006; 21(4): 203 - 208. [Abstract] [PDF]

				Y. Abu-Omar and C. Ratnatunga Cardiopulmonary Bypass and Renal Injury Perfusion, July 1, 2006; 21(4): 209 - 213. [Abstract] [PDF]

				C. W. Hogue Jr, C. A. Palin, and J. E. Arrowsmith Cardiopulmonary bypass management and neurologic outcomes: an evidence-based appraisal of current practices. Anesth. Analg., July 1, 2006; 103(1): 21 - 37. [Abstract] [Full Text] [PDF]

				P. M. Bokesch, G. A. Izykenova, J. B. Justice, K. A. Easley, and S. A. Dambinova NMDA Receptor Antibodies Predict Adverse Neurological Outcome After Cardiac Surgery in High-Risk Patients Stroke, June 1, 2006; 37(6): 1432 - 1436. [Abstract] [Full Text] [PDF]

				B. Bronden, M. Dencker, M. Allers, I. Plaza, and H. Jonsson Differential Distribution of Lipid Microemboli After Cardiac Surgery Ann. Thorac. Surg., February 1, 2006; 81(2): 643 - 648. [Abstract] [Full Text] [PDF]

				G. M. McKhann, M. A. Grega, L. M. Borowicz Jr, W. A. Baumgartner, and O. A. Selnes Stroke and Encephalopathy After Cardiac Surgery: An Update Stroke, February 1, 2006; 37(2): 562 - 571. [Abstract] [Full Text] [PDF]

				D Belway, F D Rubens, D Wozny, B Henley, and H J Nathan Are we doing everything we can to conserve blood during bypass? A national survey Perfusion, September 1, 2005; 20(5): 237 - 241. [Abstract] [PDF]

				A. Khosravi, C. A Skrabal, B. Westphal, G. Kundt, B. Greim, E. Kunesch, A. Liebold, and G. Steinhoff Evaluation of coated oxygenators in cardiopulmonary bypass systems and their impact on neurocognitive function Perfusion, September 1, 2005; 20(5): 249 - 254. [Abstract] [PDF]

				H. P. Grocott, H. M. Homi, and F. Puskas Cognitive Dysfunction After Cardiac Surgery: Revisiting Etiology Seminars in Cardiothoracic and Vascular Anesthesia, June 1, 2005; 9(2): 123 - 129. [Abstract] [PDF]

				K. Prasongsukarn and M. A. Borger Reducing Cerebral Emboli During Cardiopulmonary Bypass Seminars in Cardiothoracic and Vascular Anesthesia, June 1, 2005; 9(2): 153 - 158. [Abstract] [PDF]

				H. P. Grocott S100{beta} and postcardiac surgery neurological dysfunction: reasons to disregard any link Can J Anesth, April 1, 2005; 52(4): 441 - 442. [Full Text] [PDF]

				E. Sirvinskas, T. Lenkutis, L. Raliene, A. Veikutiene, J. Vaskelyte, and I. Marchertiene Influence of residual blood autotransfused from cardiopulmonary bypass circuit on clinical outcome after cardiac surgery Perfusion, March 1, 2005; 20(2): 71 - 75. [Abstract] [PDF]

				H. Jonsson, A. Nilsson, F. Petersson, M. Allers, and T. Laurell Particle separation using ultrasound can be used with human shed mediastinal blood Perfusion, January 1, 2005; 20(1): 39 - 43. [Abstract] [PDF]

				S Svenmarker, K G Engstrom, T Karlsson, E Jansson, R Lindholm, and T Aberg Influence of pericardial suction blood retransfusion on memory function and release of protein S100B Perfusion, December 1, 2004; 19(6): 337 - 343. [Abstract] [PDF]

				J. M. Murkin Postoperative cognitive dysfunction: aprotinin, bleeding and cognitive testing/Dysfonction cognitive postoperatoire : aprotinine, hemorragie et epreuves cognitives Can J Anesth, December 1, 2004; 51(10): 957 - 962. [Full Text] [PDF]

				S. Bar-Yosef, M. Anders, G. B. Mackensen, L. K. Ti, J. P. Mathew, B. Phillips-Bute, R. H. Messier, H. P. Grocott, and the Neurological Outcome Research Group and CARE I Aortic Atheroma Burden and Cognitive Dysfunction After Coronary Artery Bypass Graft Surgery Ann. Thorac. Surg., November 1, 2004; 78(5): 1556 - 1562. [Abstract] [Full Text] [PDF]

				H. Jonsson, C. Holm, A. Nilsson, F. Petersson, P. Johnsson, and T. Laurell Particle Separation Using Ultrasound Can Radically Reduce Embolic Load to Brain After Cardiac Surgery Ann. Thorac. Surg., November 1, 2004; 78(5): 1572 - 1577. [Abstract] [Full Text] [PDF]

				H. P. Grocott Invited commentary Ann. Thorac. Surg., July 1, 2004; 78(1): 52 - 53. [Full Text] [PDF]

M. Westerberg, A. Bengtsson, and A. Jeppsson Coronary surgery without cardiotomy suction and autotransfusion reduces the postoperative systemic inflammatory response Ann. Thorac. Surg., July 1, 2004; 78(1): 54 - 59. [Abstract] [Full Text] [PDF]