Changes in cerebral oxygen saturation with change in posture: A preliminary report

Changes in Cerebral Oxygen Saturation With Change in Posture: A Preliminary Report Mukesh Misra, MD, Manuel Dujovny, MD, M. Serdar Alp, MD, Konstantin V. Slavin, MD, James I. Ausman, MD, PhD, and Ronald A. Widman, BS

Background. Disease of the major vessels in the neck can disrupt autoregulation and lead to changes in the cerebral blood flow and cerebral autoregulation. These changes can be reflected by means of cerebral oxygen saturation. Methods. We measured cerebral oxygen saturation in 20 patients with atherosclerotic disease of the carotid and vertebral arteries and compared results with 10 normal subjects. Saturation was measured using a noninvasive near-infrared device, the transcranial cerebral oximeter. Results. There were marked decreases in cerebral oxygen saturation in patients with carotid-vertebral artery disease when the position of the patient was changed, from supine to erect. Conclusion. Changes in regional cerebral oxygen saturation inpatients with carotid-vertebral artery disease may reflect disruption of cerebral autoregulation. Key Words: Autoregulation---Carotid vertebral disease-Orthostatic test--Transcranial cerebral oximetry.

Transcranial Doppler sonography (TCD) has shown that in patients with occlusion of the internal carotid artery (ICA),1 the brain can cope with pressure drops by enhancing collateral circulation and adjustments in cerebral autoregulation. 1In addition, the brain may supply its metabolic demands by extracting more oxygen from its blood supply. 2-3 Some patients with already increased oxygen extraction due to occlusive carotid disease do have an exhausted cerebral vasomotor reactivity and are at risk for future hemodynamically related stroke. 4~ Recently, changes in regional oxygen saturation (rSO2) that occur when a patient with atherosclerotic stenosis of ICA and middle cerebral artery changes position has been reported by Slavin et al. in their clinical experience with transcranial cerebral oximetry (TCCO). 6 To the best of our knowledge, there has been no study published showing changes in cerebral oxygen saturation in patients with impaired cerebral autoregulation by using TCCO, al-

From the Department of Neurosurgery, University of Illinois at Chicago,Chicago,IL. Received November27,1995;acceptedDecember13,1996. Address reprint requests to Manuel Dujovny,MD, Department of Neurosurgery (M/C 799),The University of Illinoisat Chicago,912 S. WoodSt, Chicago,IL60612-7329. Copyright 9 1997by National StrokeAssociation 1052-3057/97/0605-000653.00/0

though dysautoregulation in patients with central neurogenic orthostatic hypotension (Shy-Drager syndrome) has been studied. 7 We describe postural changes in rSO2 of patients with carotid-vertebral artery disease using TCCO.

Methods Techniques The cerebral oximeter (INVOS 3100 A; Somanetics Troy, MI) monitors rSO2 in microvascular structures of the brain by noninvasive means. 8 It uses near-infrared spectroscopy (NIRS) for detection of regional hemoglobin oxygen saturation, providing a convenient technique to indirectly monitor adequacy of cerebral blood flow (CBF). The cerebral oximeter consists of a display unit, preamplitier, and disposable sensor pads. The dual detector-sensor measures photon return at two distances from the light source, corresponding to two depths of penetration. 9 The light source emits light in the near-infrared range (700 to 900 run) and illuminates the tissue. The intensity of light received by each detector is converted to an electrical signal for further processing by the preamplifier and display unit. 1~The oxygen saturation value is displayed on-screen as a percentage and a trend (with up to 24-hours duration). In addition, saturation data can be archived on disk using the optional disk drive accessory.

Journal of Stroke and Cerebrovascular Diseases, Vol. 6, No. 5, 1997: pp 337-340

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338

Clinical Management

Twenty patients with symptoms of carotid or vertebral ischemia evaluated by digital subtraction angiography were included in this study (Fig 1); 11 had unilateral carotid artery disease and 5 had bilateral carotid disease, 3 had unilateral carotid and vertebral artery disease, and 2 had bilateral carotid and vertebral artery disease. Twelve patients had systemic hypertension and 6 had late onset diabetes mellitus. Two patients had coronary bypass surgery performed in the past. The patients being treated individually for hypertension and diabetes, and 4 patient were on aspirin at the time of examination. Ten individuals having no known neurological or cerebrovascular disorder were used as a control population. There were 8 women and 12 men in the study group with age ranging from 47 to 77 years with a mean of 56 years. There were 5 women and 5 men in the control group with the mean age of 50 years. None of the subjects in either group were on medication that could induce postural hypotension; however, there were several patients with carotid artery disease who complained of symptoms suggestive of postural hypotension. The symptoms and signs of the patients in the study were suggestive of stroke, transient ischemic attack in the anterior circulation, or vertebrobasilar territory. Patient and control groups rSO2 was measured along with blood pressure and pulse in supine, sifting, and standing positions for 10 minutes in each position. After monitoring these patients with the transcranial cerebral oximeter (TCCO) the data were collected and processed.

Figure 1. Cerebralangiogram of patient in the study showing severe carotid stenosis. A

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Figure 2. (A) Representative graph of contim~ous regional cerebral oxygen saturation during position changes of a control subject. Other control graphs show similar graphic pattern. (B) Representative graph of continuous regional cerebral oxygen saturation during position changesfor patient 1. Other patient graphs show similarvariabilih/.

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Table 1. Percent change in regional cerebral o.rvgen saturation (Mean +- SD) during position changes in patients and controls Position change

Patients

Controls

Supine to sitting Sitting to standing Standing to supine

-9.87 --- 6.83* -6.81 __+4.83* + 19.79 --+ 12.08"

-0.52 --- 1.06 - 1.06 --- 1.90 +0.74 -+ 1.16

*Significantly different from controls (P < .002) A representative graph of 1 control and I patient is shown in Fig 2A and 2B, respectively. Before beginning the tests, a self-adhesive oxygen saturation sensor was placed on each subject either right or left of midline just below the hairline. These sensors incorporate a light source and two detectors spaced 3 and 4 crn from the light source. The signals from the proximal detector, which samples a shallower mean depth of penetration, are used to correct signals from the distal detector to suppress the effects of extracerebral blood and tissue on the measurement. The geometry of the sensors allows the measurement of regional blood oxygen saturation predominantly from the frontal cortex 3 in an area supplied by both markers between the anterior and the middle cerebral arteries.

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Data A n a l y s i s

Data from the cerebral oximeter were sampled approximately four times a minute, stored on disk, and analyzed off-line. Values for each patient's regional oxygen saturation were calculated as the average of all readings for each position. All patients' means for each position were compared with the means from the previous position using single-factor analysis of variance (ANOVA) to establish significance of the change (Fig 3). Student's t test was used to compare means from patients in each position with means from controls to establish significance. Mean percentage change was calculated for each transition and patients were compared to controls also using the t test. Results

Compared with controls, for patients with carotid and vertebral artery disease, we recorded significant reduction in rSO2 when patients were asked to sit from the supine position and a further decline when patients were asked to stand (Table 1). The fall in rSO2 occurred almost immediately after the positional change and remained at this decreased level as long as patients held their position. The rSO2 recordings returned to baseline when the patient

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Figure 4. Mean values of cerebral oxygen saturation for patients (0 n = 20) and controls ( 0 n = 10) during change in position. *Patient values that are significantly different from preceding vahtes, P < .001. #Patient values that are significantly different from controls P < .005.

340 returned to supine position after standing. Some controls experienced brief and minor falls in rSO2 as a result of position change. The mean difference in the patients and the controls during position change is shown in Fig 4. The changes documented in the pulse and blood pressure did not follow any consistent definitive pattern. However, a drop in blood pressure with mild tachycardia was noted only in some of the patients. There was no such findings in the control group.

Discussion In this study, patients had major carotid or vertebral artery disease or both. Sixteen of the 20 patients had more than 90% stenosis of either of the vessels in the neck. Otherwise, the severity of the stenosis ranged upward from 65% or there was occlusion in at least one of the carotid or vertebral arteries. The rSO2 measured by TCCO fell significantly from supine to sitting and then decreased further on standing erect, only returning to baseline after patients resumed the supine position. These findings suggest disturbances of cerebral autoregulation and infer alterations in the CBF in those subjects. Unlike pulse oximetry, the TCCO unit measures oxygen saturation of all the blood in the field of view. Because the relative distribution of venous to arterial blood in tissue is about 3:1,11 the rSO2 value reflects predominantly venous blood oxygen saturation, which can be affected by changes in blood oxygenation, CBF, metabolic rate, and blood hemoglobin content. During testing, we assumed there were no major changes in arterial oxygen saturation, metabolic rate, or hemoglobin. Therefore, the changes in rSO2 that were recorded may be primarily attributed to changes in regional CBF in the area of the oxygen sensor. Our data do not provide information on the mechanisms of the dysautoregulation. In conclusion, our findings suggest that brain oxygen saturation may not remain constant during changes in posture in patients with cerebrovascular insufficiency. These preliminary findings are suggestive of disrupted cerebral autonomic regulation in patients with carotidvertebral artery disease. Also, the transcranial cerebral oximeter may be of great value in screening, confirming

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and assessing the severity of cerebral autoregulation in such patients.

Acknowledgment: We sincerely thankJulie Bedore White for editing our manuscript. References 1. Keunen RWM, Akerstaff RGA, Stegeman DF, Schulte BPM. The impact of internal carotid artery occlusion and of the integrity of the circle of Wilhs on cerebral vasomotor reactivity--a transcranial Doppler study. Proceedings of 14th International Salzburg Conference on Cerebrovascular Disease, Salzburg, Austria, 1988. 2. Power WJ, Press GA, Grubb RL, Gad M, Raichle ME. The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation. Ann Intern Med 1987;106:27-35. 3. Herold WJ, Brown MM, Frackowiak RSJ, Mansfield AO, Thomas DJ, Marshall J. Assessment of cerebral hemodynamic reserve: correlation between PET parameters and C O 2 reactivity measured by intravenous 133 Xe injection technique. J Neurol Neurosurg Psychiatry 1988;51:10451050. 4. Kleiser B, Widder B: Course of carotid artery occlusions with impaired cerebrovascular reactivity. Stroke 1992;23: 171-174. 5. Yonas H, Smith HA, Durham SR, Pentheny SL, Johnson DW. Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 1993;79:483489. 6. Slavin KV, Dujovny M, Ausman IJ, Hernandez G, Leur M, Stoddart H. Clinical experience with transcranial cerebral oximetry. Surg Neurol 1994;42:531-40. 7. Meyer JS, Shimazu K, Fukuuchi Y, Ohuchi T, Okamoto S, Koto A, Ericsson AD. Cerebral dysautoregulation in central neurogenic orthostatic hypotension (Shy-Drager syndrome). Neurology 1973;23:262-273. 8. Dujovny M, Slavin KV, Cui W, Lewis G, Ausman Jh Somanetics INVOS 3100 cerebral oximeter. Neurosurgery 1994;34:935-936. 9. Cui W, Kumar C, Chance B. Experimental study of migration depth for the photons measured at sample surface. SPIE 1991:1431. 10. McCormick PW, Stewart M, Goetting MG, Balakrishnan G. Regional cerebrovascular oxygen saturation measured by optical spectroscopy in humans. Stroke 1991;22:596601. 11. Mchedhshvilli GI. Arterial behavior and blood circulation in the brain. New York: Plenum, 1986:56-57.