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Eur J Cardiothorac Surg 2004;25:401-406
© 2004 Elsevier Science NL

Using jugular bulb oxyhemoglobin saturation to guide onset of deep hypothermic circulatory arrest does not affect post-operative neuropsychological function

Departments of Anesthesiology and Biomathematical Sciences, Mount Sinai School of Medicine, New York, NY 10029, USA

Received 4 June 2003; received in revised form 23 October 2003; accepted 27 November 2003.

^* Corresponding author. Address: Department of Anesthesiology, Box 1010, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, NY 10029-6574, USA. Tel.: +1-212-241-7467; fax: +1-212-241-1847
e-mail: david.reich{at}msnyuhealth.org

	Abstract

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

 
Objectives: Deep hypothermic circulatory arrest (DHCA) is commonly used during thoracic aortic surgery, and is initiated only after a sufficient degree of cerebral hypothermia is induced. The criteria for initiating DHCA vary among institutions: most centers use temperature criteria, some use electroencephalography, and a minority use jugular bulb oxyhemoglobin saturation SjO₂ criteria. The purpose of this study was to determine whether the use of SjO₂ monitoring to guide the onset of DHCA was associated with better post-operative neuropsychological outcome. Methods: Sixty-one thoracic aortic surgical patients underwent both pre- and post-operative neuropsychological testing. Patients were divided into three groups: (1) those with SjO₂95% at DHCA onset; (2) those with SjO₂<95% at DHCA onset; and (3) those without SjO₂ monitoring. Results: There were no statistically significant differences in the incidence of post-operative decline in neuropsychological function among the three groups of patients. Patients in whom SjO₂ data were used to guide onset of DHCA had lower esophageal and bladder temperatures at that time compared with patients without SjO₂ monitoring. Conclusions: Monitoring of SjO₂ had no apparent effect upon post-operative neuropsychological outcome, and there were no trends in our small patient cohort suggesting differences that our study was not adequately powered to detect. Use of SjO₂ monitoring was associated with more profound hypothermia prior to DHCA due to more prolonged cooling in attempts to bring the SjO₂ above the 95% threshold. Using our institutional cooling protocol, SjO₂ monitoring does not appear to increase neuroprotection in patients undergoing DHCA for thoracic aortic repairs.

Key Words: Aortic aneurysm • Thoracic • Thoracic surgery • Neuropsychology • Outcome study • Hypothermic circulatory arrest • Jugular bulb oxyhemoglobin saturation

	1. Introduction

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

 
Thoracic aortic surgery often requires that blood flow to the brain be interrupted for some period of time during the repair. In order to prevent global cerebral ischemic injury, a state of deep hypothermia is induced via cardiopulmonary bypass (CPB) prior to initiating circulatory arrest. Reductions in cerebral metabolism, rate of ATP depletion, release of toxic neurotransmitters, generation of free radicals, and reperfusion injury are among the mechanisms that are believed to underlie the neuroprotective effect of hypothermia during and after deep hypothermic circulatory arrest (DHCA) [1].

As the cerebral metabolic rate for oxygen decreases and the affinity of hemoglobin for oxygen increases with hypothermia, less oxygen is extracted from the blood and the oxyhemoglobin saturation of the venous effluent from the brain increases [2]. We have monitored SjO₂ as a marker of global cerebral hypothermia so as to optimize neuroprotection prior to instituting DHCA. Our institution is one of the few that uses SjO₂ of 95% or greater as one of the criteria for initiating DHCA in adults undergoing thoracic aortic surgery.

At many institutions, temperature-based cooling criteria are the norm, however, clinical and animal research suggests that temperatures measured at standard extracranial monitoring sites (i.e. rectal, bladder, esophageal, nasopharyngeal and tympanic) do not reflect brain temperature during induction of hypothermia [3–5]. Furthermore, certain brain regions have a greater cerebral blood flow than others (e.g. gray matter vs. white matter), and it is reasonable to expect that those brain regions that have higher blood flow will cool more rapidly. Some institutions use electroencephalographic (EEG) monitoring to document electrical silence prior to the onset of DHCA. EEG is, however, a surface monitor and does not reflect the physiological activity of deeper structures, which may not be cooled to the same degree as the cerebral cortex.

Our standard approach has been to use both SjO₂ and temperature monitoring to guide the onset of DHCA. Using this methodology, we often had to cool patients on cardiopulmonary bypass for longer periods of time to raise the SjO₂ above the 95% threshold than we would have, had we used temperature criteria alone. In some patients, however, we have cooled using only temperature criteria, because the SjO₂ catheter was not functioning properly or could not be inserted for technical reasons. In this retrospective investigation, we sought to determine whether the presence of a functional SjO₂ catheter and use of the SjO₂ data to guide the onset of DHCA led to better neuroprotection.

	2. Materials and methods

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

 
Under an Institution Review Board approved protocol with informed consent, patients undergoing elective thoracic aortic surgery were evaluated with a battery of neuropsychological tests pre-operatively (n=124) and at the post-operative outpatient follow-up visit (n=61).

The surgical technique for induction of profound hypothermia and use of circulatory arrest was constant throughout the duration of the study, and has been described in detail previously [6]. Briefly, central cooling on cardiopulmonary bypass was carried out using alpha-stat blood gas management to produce profound total body hypothermia to a core temperature of 12–15 °C, as measured in the esophagus. In adults, a minimum duration of 30 min is usually required for cooling that is thorough enough to prevent upward drift of body temperature during prolonged HCA.

Using superficial landmarks and/or an ultrasonic vessel locating system (Site Rite, Bard Access Systems, Pittsburgh, PA), the internal jugular vein was cannulated with a 1.5 cm 20-gauge catheter aimed in a cephalad direction. Using the Seldinger technique, the short catheter was exchanged over a guide wire to a 12 cm 20-gauge catheter that was inserted to a length of 10–11 cm. The external portion of the catheter was then looped 180°, such that the hub faced cephalad, and was then sutured carefully to prevent kinking and attached to a transducer-flush system. A baseline blood sample was drawn to confirm that the oxyhemoglobin saturation was consistent with location of the distal end of the catheter in the jugular bulb (oxyhemoglobin saturation <70%). All SjO₂ determinations were made with a point-of-care arterial blood gas device that measured pO₂ and calculated the oxyhemoglobin saturation using a nomogram (Gem Premier, Mallinckrodt Sensor Systems, Hazelwood, MO).

The length of time of hypothermic CPB prior to initiating DHCA varied widely according to the needs of the particular thoracic aortic repair. In patients where the initial portion of the aortic repair did not require DHCA (e.g. the aortic valve annulus anastomosis and coronary reimplantations of the Bentall Procedure), the patients were cooled to an esophageal temperature of 15–20 °C and maintained at that level. Profound central cooling prior to DHCA was performed with perfusate temperatures of approximately 10 °C. During this profound cooling, we measured SjO₂ every 5 min. DHCA was usually implemented when the SjO₂ was 95% or greater, but was implemented at SjO₂ values less than 95% when prolonged cooling (>30 min) failed to cause further increases in SjO₂. Except for straightforward distal ascending aortic anastomoses expected to take less than 20 min, the head was always packed in ice prior to the period of profound cooling and DHCA to prevent warming of the brain by ambient room temperature.

Upon reinstitution of cerebral perfusion and completion of the aortic repair, gradual rewarming was carried out by means of cardiopulmonary bypass, limiting the gradient between blood and body temperature to less than 10 °C, with a maximum blood temperature of 37 °C. A warming blanket was also utilized. Central warming was usually discontinued at an esophageal temperature of 35–37 °C and a rectal or bladder temperature of 30–35 °C.

All patients were given 30 mg kg^-1 of methylprednisolone prior to DHCA. Glucocorticoids were continued in tapering doses for 48 h in those patients with an interval of DHCA exceeding 30 min. Recovery occurred in the intensive care unit.

Patients were evaluated for gross neurological deficits upon emergence from anesthesia and throughout the intensive care unit stay. Neurological deficits were classified into three types: focal neurologic deficits that persisted to the time of hospital discharge (permanent stroke), focal neurologic deficits that were transient and resolved by the time of hospital discharge (transient stroke), and temporary neurological dysfunction (TND), defined as post-operative confusion, agitation, delirium, prolonged obtundation, or Parkinsonism without localizing neurological signs.

Demographic and peri-operative data collected included age, gender, cardiopulmonary bypass time, and cerebral ischemia time. Esophageal and core (bladder or rectal) temperatures and SjO₂ were measured just prior to the onset of DHCA.

2.1. Neuropsychological evaluation
All patients underwent neuropsychological evaluations by a psychologist trained in these techniques who was blinded to the clinical aspects of the surgical procedure. In order to assure that patients were not globally impaired to the extent that neuropsychological testing would be invalid, a brief orientation screen was administered (Orientation subtest of the Wechsler Memory Scale—Revised, The Psychological Corporation, San Antonio, TX). No patients were excluded on this basis. The neuropsychological battery consisted of eight tests measuring function in five domains:

1. Attention: WAIS-R Digit Span subtest (Wechsler Adult Intelligence Scale—Revised, Psychological Corporation, New York, NY);
   
2. Processing speed: The Trail Making Test, Part A (Halstead–Reitan Neuropsychological Test Battery, Neuropsychology Press, Tucson, AZ) and the Symbol Digit Modalities Test, oral version (Symbol Digit Modalities Test, Western Psychological Services, Los Angeles, CA);
   
3. Memory: The Logical Memory subtest (Wechsler Memory Scale—Revised, The Psychological Corporation, San Antonio, TX) and the Verbal Paired Associates subtest (Wechsler Memory Scale—Revised, The Psychological Corporation, San Antonio, TX). Alternate forms of these tests were used for pre-operative and post-operative testing to avoid practice effects;
   
4. Executive function: The Trail Making Test, Part B (The Halstead–Reitan Neuropsychological Test Battery, Neuropsychology Press, Tucson, AZ) and the WAIS-R Similarities subtest (Wechsler Adult Intelligence Scale-Revised, Psychological Corporation, New York); and
   
5. Fine motor function: The Finger Tapping Test (Psychological Assessment Resources, Inc., Odessa, FL) and the Grooved Pegboard Test (Psychological Assessment Resources, Inc., Odessa, FL). The dominant hand was tested.
   

Neuropsychological testing was performed pre-operatively and at the post-operative visit to the surgeon's office several weeks following surgery.

2.2. Data analysis
Patients were divided into three groups: (1) those with SjO₂95% at the time of DHCA onset, (2) those with SjO₂<95% at the time of DHCA onset, and those without SjO₂ monitoring. Categorical demographic and peri-operative data were compared among the three groups of patients using ²-tests. Esophageal and core temperatures as well as continuous demographic data were compared using Kruskal–Wallis tests.

The initial step in the neuropsychological data analysis was the transformation of raw test scores into standard scores (Z-scores). This was accomplished by subtracting the baseline sample mean from the individual raw test score and dividing this difference by the baseline sample standard deviation. For timed tests, the sign was reversed. Our baseline cohort consisted of 124 patients who underwent pre-operative neuropsychological testing. The transformation of raw test scores into standard scores allowed us to combine data from different tests within a cognitive domain into composite scores, defined as the average Z-score for all tests (for which data were available) within each domain. For example, Z-scores for the Trail Making Test and Symbol Digit Modalities Test were averaged to produce the processing speed composite score. Thus, the volume of neuropsychological data was reduced to five pre-operative and five post-operative cognitive domain composite scores for each patient. Post-operative change for each patient and each domain was then defined as the difference between the pre- and post-operative composite scores.

For each domain, patients were then classified as either experiencing a significant post-operative decline in function (defined as a decrease in the composite score of one standard deviation or greater) or not. Finally, a general measure of negative neuropsychological outcome (NNO) was defined as a post-operative decrease of one standard deviation or more in at least two domains (for patients with data in at least three domains). The relationship between patient group and binary neuropsychological data was analyzed by ²-tests.

	3. Results

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

 
The three groups of patients (SjO₂95%, SjO₂<95%, or no SjO₂ monitoring) did not differ with respect to age, gender, cardiopulmonary bypass time, or cerebral ischemia time, when considering either the entire sample of patients that had pre-operative neuropsychological testing, or the subset that had both pre- and post-operative neuropsychological testing (see Tables 1 and 2). The three groups did, however, differ with respect to both esophageal and core temperatures. In patients without SjO₂ monitoring (group 3), both core and esophageal temperatures were higher than in patients with SjO₂ monitoring (groups 1 and 2; see Fig. 1) .

View larger version (11K): [in this window] [in a new window]   Fig. 1. Core temperature (rectal or bladder) prior to deep hypothermic circulatory arrest in patients undergoing thoracic aortic surgery (abbreviation: SjO2, jugular venous oxyhemoglobin saturation).

Post-operative neuropsychological testing occurred at a median of 67 days following surgery (range 7–127 days); there was no difference in time to follow-up between the three groups (see Table 2). For 12 patients, the complete battery of tests was not administered either pre-operatively or post-operatively, due to patients' request to discontinue testing or interruptions by other hospital activities. Fifty-four patients had at least three domains tested both pre- and post-operatively and entered into the analysis of NNO. Of the 61 patients with post-operative testing, 43 also had jugular bulb oxyhemoglobin monitoring (SjO₂95% n=26, 43%; SjO₂<95% n=17, 28%; and no SjO₂ data n=18; 29%). There were no statistically significant differences in post-operative neuropsychological decline between patients whose onset of DHCA was guided by SjO₂ data vs. patients without SjO₂ data, either for the specific cognitive domains or overall neuropsychological function (i.e. NNO; see Table 3). Among patients with SjO₂ data, there were no statistically significant differences in post-operative neuropsychological outcome between patients in whom SjO₂ reached 95% prior to initiating circulatory arrest vs. patients in whom SjO₂ failed to reach 95% prior to DHCA. There also was no evidence of any trends suggesting differences that our study was too small to detect (see Table 3).

	4. Discussion

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

Both TND and post-operative decline in neuropsychological function are believed to result from inadequate cerebral protection; the incidence of both forms of cerebral injury increases with duration of DHCA, as well as patient age [5,7]. The fact that SjO₂ status was not associated with either of these two outcomes strongly suggests that there was no difference among the three groups in terms of adequacy of cerebral protection before initiating DHCA.

In the absence of any difference or trends suggesting that our patients without SjO₂ monitoring had worse neuropsychological outcomes or a higher incidence of TND, the temperature-based cooling criteria at our institution seem to have provided sufficient cerebral protection. The temperature-based cooling criteria that we used in the absence of SjO₂ data induce hypothermia that is more profound than at many comparable institutions. Typically, in the period immediately preceding DHCA, we have employed a bath temperature of 4 °C, resulting in a perfusate temperature of 10–12 °C. We continue cooling in this fashion until the esophageal temperature is 12–15 °C and the bladder temperature is 15–18 °C prior to instituting DHCA.

The use of SjO₂ monitoring (groups 1 and 2) was associated with cooler esophageal and bladder temperatures prior to DHCA onset, likely due to longer durations of cooling in these patients. However, we cannot analyze the total cooling times directly, because the heterogeneity of the surgical procedures necessitated various cooling strategies and variable timing of DHCA within the period of CPB. For example, patients undergoing the Bentall procedure were typically cooled to a temperature of 20 °C for the aortic root and coronary artery anastomoses, and then cooled further for the distal aortic anastomosis under DHCA. In contrast, transverse aortic arch repairs required DHCA soon after the initiation of CPB as a sufficient degree of hypothermia was established.

It has been shown that episodes of cerebral venous desaturation (defined as an SjO₂<50% or pO₂<25 mmHg) associated with reduced cerebral perfusion following severe traumatic brain injury are associated with poor neurologic outcome [8]. The relationship between episodes of desaturation during various phases of cardiac surgery with hypothermic cardiopulmonary bypass (but not DHCA) and post-operative neuropsychological function has also been studied. Desaturation occurs most frequently during the rewarming phase of CPB, and is believed to reflect a mismatch between cerebral perfusion and metabolic needs. The results of these studies have been divergent, but this may be due to differences in the methodology of cognitive testing (i.e. time of post-operative testing and tests utilized). Croughwell et al. [9] found that jugular bulb desaturation (defined as an SjO₂<50% or pO₂<25 mmHg) during rewarming was related to post-operative cognitive decline measured 4–8 days following surgery using a battery of nine tests. All functional domains were affected; there was no selective impairment. Robson et al. [10] found no relationship between intraoperative and post-operative episodes of desaturation and post-operative cognitive decline measured 3 months after surgery using a battery of 11 tests. In contrast, Yoshitani et al. [11] found that high SjO₂ levels 10 min after start of surgery and at 30 °C during rewarming predicted cognitive decline 10–14 days following cardiac surgery with hypothermic CPB using a brief mental status test and a test of visual memory. Therefore, there is no consensus regarding the validity of SjO₂ as a marker for neurological outcome following cardiac surgery.

The value of SjO₂ data must be considered in light of the limitations of venous saturation monitoring. In addition to decreasing cerebral metabolic rate, hypothermia increases the solubility of oxygen in blood and the affinity of hemoglobin for oxygen (reduced P₅₀), both of which may adversely affect oxygen delivery to brain tissue and increase the oxyhemoglobin saturation of the venous effluent. Thus, neuronal hypoxia may exist despite normal or elevated SjO₂ values if neurons are unable to adequately extract oxygen from the blood during extreme hypothermia. Additionally, variable degrees of arteriovenous shunting and extracranial contamination confound the interpretation of SjO₂ as an index of cerebral venous oxyhemoglobin saturation. Moreover, mechanisms other than metabolic suppression probably also contribute to hypothermia's neuroprotective effect. For example, inhibition of excitotoxic neurotransmitter release and reperfusion injury are factors that may be as or more important than cerebral metabolic suppression. For these reasons, we have always considered elevated SjO₂ values during hypothermic perfusion prior to DHCA as a marker of sufficient global brain cooling, rather than a direct reflection of cerebral oxygen metabolism at the cellular level or an index of the brain's ability to tolerate an ischemic insult.

One of the limitations of this long-term follow-up study of neuropsychological function following thoracic aortic surgery is the high attrition rate. As a tertiary care center where these patients are referred, many patients do not return for the post-operative visit that is usually scheduled 4–6 weeks following surgery. The geographical distance is often quite large and many patients chose to be followed by physicians nearer to their residence. Based upon our experience, the attrition is mainly related to this factor. A greater proportion of patients who were lost to follow-up, however, had post-operative TND, which has been shown to be associated with long-term post-operative neuropsychological dysfunction [12]. We have no way of determining the proportion of patients who had neuropsychological dysfunction in the portion of the cohort that was lost to follow-up.

In light of the limitations of this retrospective analysis, we have not discontinued our use of jugular bulb oxyhemoglobin monitoring in thoracic aortic surgery, but are less concerned when prolonged cooling fails to raise the SjO₂ above the 95% threshold. The technical ease and lack of complications associated with jugular bulb catheterization are such that no significant cost or time savings would result from discontinuation of SjO₂ monitoring. Furthermore, analysis of a larger cohort of patients with SjO₂<90% in the future may yield further information.

It is unlikely that cerebral hypothermia beyond the levels used in our institution confers additional neuroprotection in the thoracic aortic surgical population. Other methods must be explored to reduce the significant incidence of TND and neuropsychological dysfunction in thoracic aortic surgery requiring DHCA [6,13]. We are currently evaluating the use of right axillary artery cannulation, performing a separate graft to the brachiocephalic arteries (e.g. Tanaguchi procedure), and selective cerebral perfusion to reduce the period of cerebral ischemia in aortic arch reconstructions [14].

In conclusion, SjO₂ monitoring and attempts to achieve SjO₂95% prior to the onset of DHCA do not appear to improve neurological or neuropsychological outcome following thoracic aortic surgery requiring DHCA with the profound cooling regimen at the authors' institution. Further investigation will be required to determine if lower SjO₂ thresholds have prognostic significance in DHCA patients.

	Footnotes

 
¹ Consulting statisticians.

	References

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

 

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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 Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Reich, D. L. Articles by Uysal, S. Search for Related Content PubMed PubMed Citation Articles by Reich, D. L. Articles by Uysal, S. Related Collections Anesthesia Cerebral protection Extracorporeal circulation Great vessels Related Article