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Evaluation of cerebral hemodynamics in a head-injured patient with hypovolemia using transcranial doppler sonography
Evaluation of Cerebral Hemodynamics in a Head-Injured Patient With Hypovolemia Using Transcranial Doppler Sonography KOJI IIDA, MD,* KAORU KURISU, MD,* KAZUNORI ARITA, MD,* TOSHINORI NAKAHARA, MD,* MINAKO OHTANI, MD,I" HIDEKI SATOH, MD'I" A 20-year-old man presented with hypovolemic shock caused by abdominal injury. Cerebral hemodynamics were evaluated by transcranial Doppler (TCD) sonography. Middle cerebral artery flow velocities decreased, and the pulsatility indices increased markedly. Particularly, the waveform of the left middle cerebral artery showed a systolic peak, suggesting an increased intracranial pressure. Actual intracranial pressure was 7 mm Hg, and the cerebral perfusion pressure (CPP) was 51 mm Hg. These abnormal Doppler signals seemed to be caused by a compromise in CPP and to be aggravated by hypovolemia. The patient was discharged with a residual mild memory disturbance. Hypovolemia aggravates a reduced cerebral blood flow caused by a compromised CPP, and the waveform of TCD in a case of hypovolemic shock should be differentiated from intracranial hypertension. (Am J Emerg Meal 1997;15:587-590. Copyright © 1997 by W.B. Saunders Company) Hypovolemic shock accompanied by head injury can lead to serious consequences. However, little is known about cerebral hemodynamics in that state. We report the case of a patient with multiple injuries, including head injury, who suffered from hypovolemic shock, and assessed the cerebral hemodynamic changes using transcranial Doppler (TCD) sonography.
CASE REPORT A 20-year-old man was transferred to the Department of Neurosurgery, Hiroshima University Hospital on December l l, 1993 for the treatment of multiple injuries resulting from a traffic accident. On admission, the patient had a Glasgow Coma Scale score of 7 (El V1 M5), and showed isocoric pupils with an intact light reflex. No paresis of his extremities was observed. There were bruises on his face and forehead. Examination of his abdomen showed mild guarding. His systolic arterial pressure (sAP) was 70 mm Hg; diastolic arterial pressure (dAP), 37 mm Hg; and heart rate, 127 beats/min. Because the patient's consciousness had been impaired since the accident, a serious intracranial lesion was suspected. However, cranial computed tomography (CT) showed no lesions (Figure 1). A pulmonary contusion and a pneumothorax were shown with chest CT (Figure 2A), and a hepatic parenchymal From the *Department of Neurosurgery and Division of Emergency Medicine and I-Intensive Care Medicine, Hiroshima University School of Medicine, Hiroshima, Japan. Manuscript received March 6, 1996; accepted June 30, 1996. Address reprint requests to Dr lida, Department of Neurosurgery, Hiroshima University School of Medicine, 1-2-3 Kasumi, Minami-ku, Hiroshima 734, Japan. Key Words:Hypovolemic shock, cerebral hemodynamics, transcranial Doppler sonography, cerebral circulatory arrest, cerebral arterial collapse. Copyright © 1997 by W.B. Saunders Company 0735-6757/97/1506-0011 $5.00/0
hematoma and a hemoperitoneum were shown with abdominal CT (Figure 2B). TCD examination disclosed abnormal Doppler signals, initially thought to reflect intracranial hypertension. The middle cerebral artery flow velocities (MCAFVs) were markedly decreased (fight, 24 crrdsec; left, 10 cm/sec), and the pnlsatility indices significantly increased (right, 2.21; left, 4.29) (Figure 3). The diastolic flow signal of the left middle cerebral artery (MCA) was especially diminished. The internal carotid artery flow velocities (ICAFVs), insonated in the neck, were also decreased. However, the intracranial pressure (ICP) was normal at 7 mm Hg, and the cerebral perfusion pressure (CPP) was calculated to be 51 mm Hg (sAR 84 mm Hg; dAR 45 mm Hg). Blood gas analysis showed a state of normocapnia (Paco2, 39 mm Hg; Pao> 204 mm Hg; pH, 7.2). Therefore, it was thought that these TCD findings were caused by severe hypovolemia, not by intracranial hypertension. Emergency laparotomy for the hepatic injury was performed because of sustained hemodynamic instability after conservative therapy including high volumes of intravenous infusions and multiple transfusions. The patient's preoperative hemoglobin concentration was 6.4 mg/dL, and his hematocrit was 20%. The estimated blood loss during the operation was 7,000 mL, and total volume of intravenous infusions and transfusions was 8,000 mL. Postoperatively, the systemic hemodynamics were stabilized, and the right MCAFV and ICAFV increased to normal. The left MCAFV transiently increased to 80 cngsec before decreasing to normal; this was accompanied by a similar increase in the ipsilateral ICAFV (Figure 4). Monitoring the jugular bulb oxyhemoglobin saturation (Sjo2) was started postoperatively. The initial Sjo2 was 54.7%, which increased to a maximum of 82% during a 2-day interval before returning to normal. The ICP remained within the normal range. On the third hospital day, the patient gained consciousness, and no lesion was observed with serial cranial CT and magnetic resonance imaging (MRI). The patient was discharged with a mild residual memory disturbance 2 months after admission.
DISCUSSION The evaluation of cerebral hemodynamics in critically ill patients is difficult because of the short time allowed for measurements. With the development of TCD, serial evaluation of cerebral hemodynamics can be performed noninvasively, t,2 The practical usefulness of TCD monitoring has been well documented in situations such as severe head injury, 3,4 subarachnoid hemorrhage, 5 and the other cerebral vascular diseases. 6,7 However, there are few reports concerning the assessment of cerebral hemodynamics in patients with hypovolemic shock using TCD. We had the opportunity to evaluate the cerebral hemodynamics in a critically ill patient with hypovolemic shock caused by an abdominal injury. The initial results of TCD 587
588
AMERICAN JOURNAL OF EMERGENCY MEDICINE • Volume 15, Number 6 • October 1997
FIGURE 1. Cranial CT on admission showing no lesions.
examination showed a marked decrease in the MCAFVs, with an increase in their pulsatility indices. The diastolic flow signal of the left MCA was especially diminished, and its waveform appeared as a systolic peak. 8 In patients with head injuries, a characteristic progressive change in the TCD waveform can be seen during periods of increasing ICP. 4 The first change observed is a progressive decrease in the diastolic velocity. As the ICP approaches the diastolic pressure at the level of the microcirculation, the velocity approaches zero in end diastole, indicating that all of the forward flow is occurring during systole. With further increases in the ICR the waveform shows signs of cerebral circulatory arrest such as systolic spikes, to and fro, or no flow. 8 In an experimental study on the use of TCD in cases of increased ICR 9 the diastolic part of the flow velocity spectrum started to disappear once the diastolic perfusion pressure had decreased to a negative level, In this stage, only high systolic peaks are detectable. On the basis of the results from the initial TCD examination, we suspected the presence of intracranial hypertension caused by acute brain swelling or intracranial hemorrhage, and rapidly examined the ICP during the periods of preparing the operation. However, the ICP was normal, and the diastolic cerebral perfusion pressure was calculated to be 38 mm Hg. Hypocapnia can induce vasoconstriction, causing theoretical increase in the arterial blood pressure at which the MCAFV becomes zero in a pressure-velocity relationship. 1° However, blood gas analysis showed normocapnia. Therefore, these TCD findings showing nearly cerebral circulatory arrest were attributed to the hypovolemic shock. Jorgensen et al H reported changes in the middle cerebral artery velocity and pulsatility indice during induced hypovolemic shock in nine people. The hypovolemic shock was induced by passive head-up tilt. The 50 ° head-up tilt position was maintained for 60 minutes or until development of presyncopal symptoms. In all subjects, the middle cerebral artery velocity decreased and the pulsatility indice increased
FIGURE 2. (A) Chest CT on admission showing a pulmonary contusion and pneumothorax. (B) Abdominal CT shows a hematoma in the hepatic parenchyma (arrowheads) and a hemoperitoneum (arrows).
IIDA ET AL • CEREBRAL HEMODYNAMICS IN HYPOVOLEMIC SHOCK
during maintained head-up tilt. Eight of these subjects experienced presyncopal symptoms after 33 minutes in this state; this was associated with a mean arterial pressure of 65 mrn Hg (range, 32 to 84), decreased from 91 mm Hg (range, 87 to 102) at rest. The flow velocities decreased from a mean of 54 (32 to 62) to 25 (16 to 31) cm/sec, and the pulsatility indices increased from a mean of 0.8 (0.7 to 0.9) to 1.4 (1.1 to 2.5). In one subject, arterial collapse was observed when the diastolic velocity decreased to zero, corresponding to an arterial pressure at the level of the brain of 21 mm Hg. The systolic pressure was 47 rnm Hg, and mean arterial pressure in the brain was 34 mm Hg. Giller et a112 evaluated the cerebral hemodynamics of 13 healthy normotensive hypovolemic subjects during lower-body negative pressure. The middle cerebral artery flow velocity declined by 16% _+ 4% (mean + SD), and the ratio between TCD pulsatility and
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FIGURE 3. Transcranial Doppler sonographic spectral displays obtained on admission, showing decreased MCAFVs (right [A], 24 crrdsec; left [B], 10 cm/sec) and increased pulsatility indices (PIs: right [A], 2.21; left [B], 4.29). The diastolic flow signal of the left MCA was especially diminished, although the cerebral perfusion pressure was 51 mm Hg.
FIGURE 4. Changes in MCAFV in cm/sec (0), ICAFV in crrdsec (O), Sjo2 in % (IS]), and ICP in mm Hg (A). The left MCAFV transiently increased to 80 cm/sec before returning to normal; this was accompanied by a similar increase in the ipsilateral ICAFV. The value of Sjo2 also showed transient increase during a 2-day period postoperatively, followed by a return to normal. The ICP remained within the normal range.
systemic pulsatility increased 22% + 8%. These findings suggest a possibility of a decrease in cerebral blood flow that can cause neurological deficits during hypovolemia even in patients who maintain normal blood pressures. In the present case, the appearance of the systolic peak on TCD could not have been caused by a compromised cerebral perfusion pressure alone, and also may have been secondary to severe hypovolemia. The TCD and Sjo2 findings showed a postischemic hyperemia 2 days postoperatively. The initial postoperative Sjo2 value was 54.7%, and may have been less preoperatively. Generally, a Sjo2 of less than 50% is associated with cerebral hypoxia. 13 Therefore, the patient must have suffered from cerebral ischemia more than what was caused by the cerebral perfusion pressure alone, causing a residual memory disturbance. In conclusion, hypovolemia aggravates a reduced cerebral blood flow caused by a compromised cerebral perfusion pressure, and the TCD waveforms in patients with hypovolemic shock should be differentiated from those associated with intracranial hypertension.
REFERENCES 1. Aaslid R, Markwalder TM, Nernes H: Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982;57:769-774 2. Aaslid R: Transcranial Doppler Sonography. New York, NY, Springer-Verlag, 1986 3. Chan KH, Miller JD, Dearden NM, et al: The effect of changes in cerebral perfusion pressure upon middle cerebral artery blood flow velocity and jugular bulb venous oxygen saturation after severe brain injury. J Neurosurg 1992;77:55-61 4. Newell DW, Seller RW, Aaslid R: Head injury and cerebral circulatory arrest. In Newell DW, Aaslid R (eds): Transcranial Doppler. New York, NY, Raven, 1992, pp 109-121 5. Seiler RW, Newell DW: Subarachnoid hemorrhage and vase-
590
AMERICAN JOURNAL OF EMERGENCY MEDICINE • Volume 15, Number 6 • October 1997
spasm. In Newell DW, Aaslid R (eds): Transcranial Doppler. New York, NY, Raven, 1992, pp 101-108 6. Harders A, Bien S, Eggert HR, et al: Hemodynamic changes in arteriovenous malformations induced by superselective embolization: transcranial Doppler investigation. Neurol Res 1988; 10:239-245 7. Gomez CR, Gomez SM, Yoon KWP, et al: Evaluation and follow-up of carotid-cavernous fistulas by transcranial Doppler sonography: illustrative case. Neurosurgery 1989;24:749-753 8. Hassler W, Steinmetz H, Pirschel J: Transcranial Doppler study of intracranial circulatory arrest, J Neurosurg 1989;71:195-201 9. Takaya M, Moritake K, Fukuma A, et al: An experimental study on the transcranial Doppler ultrasonography in raised intracranial pressure. In Oka M, von Reutern GM, Furuhata H, et al: (eds):
Recent Advances in Neurosonology. Amsterdam, Excerpta Medica, 1992, pp 233-237 10. Aaslid R: Cerebral hemodynamics. In Newell DW, Aaslid R (eds): Transcranial Doppler. New York, NY, Raven, 1992, pp 49-55 11. Jorgensen LG, Perko M, Perko G, et al: Middle cerebral artery velocity during head-up tilt induced hypovolaemic shock in humans. Clin Physiol 1993; 13:323-326 12. Giller CA, Levine BD, Meyer Y, et al: The cerebral hemodynamics of normotensive hypovolemia during lower-body negative pressure. J Neurosurg 1992;75:961-966 13. Cruz J: Continuous versus serial global cerebral hemometabolic monitoring: applications in acute brain trauma. Acta Neurochir Suppl (Wien) 1988;42:35-39
CASE REPORT A 20-year-old man was transferred to the Department of Neurosurgery, Hiroshima University Hospital on December l l, 1993 for the treatment of multiple injuries resulting from a traffic accident. On admission, the patient had a Glasgow Coma Scale score of 7 (El V1 M5), and showed isocoric pupils with an intact light reflex. No paresis of his extremities was observed. There were bruises on his face and forehead. Examination of his abdomen showed mild guarding. His systolic arterial pressure (sAP) was 70 mm Hg; diastolic arterial pressure (dAP), 37 mm Hg; and heart rate, 127 beats/min. Because the patient's consciousness had been impaired since the accident, a serious intracranial lesion was suspected. However, cranial computed tomography (CT) showed no lesions (Figure 1). A pulmonary contusion and a pneumothorax were shown with chest CT (Figure 2A), and a hepatic parenchymal From the *Department of Neurosurgery and Division of Emergency Medicine and I-Intensive Care Medicine, Hiroshima University School of Medicine, Hiroshima, Japan. Manuscript received March 6, 1996; accepted June 30, 1996. Address reprint requests to Dr lida, Department of Neurosurgery, Hiroshima University School of Medicine, 1-2-3 Kasumi, Minami-ku, Hiroshima 734, Japan. Key Words:Hypovolemic shock, cerebral hemodynamics, transcranial Doppler sonography, cerebral circulatory arrest, cerebral arterial collapse. Copyright © 1997 by W.B. Saunders Company 0735-6757/97/1506-0011 $5.00/0
hematoma and a hemoperitoneum were shown with abdominal CT (Figure 2B). TCD examination disclosed abnormal Doppler signals, initially thought to reflect intracranial hypertension. The middle cerebral artery flow velocities (MCAFVs) were markedly decreased (fight, 24 crrdsec; left, 10 cm/sec), and the pnlsatility indices significantly increased (right, 2.21; left, 4.29) (Figure 3). The diastolic flow signal of the left middle cerebral artery (MCA) was especially diminished. The internal carotid artery flow velocities (ICAFVs), insonated in the neck, were also decreased. However, the intracranial pressure (ICP) was normal at 7 mm Hg, and the cerebral perfusion pressure (CPP) was calculated to be 51 mm Hg (sAR 84 mm Hg; dAR 45 mm Hg). Blood gas analysis showed a state of normocapnia (Paco2, 39 mm Hg; Pao> 204 mm Hg; pH, 7.2). Therefore, it was thought that these TCD findings were caused by severe hypovolemia, not by intracranial hypertension. Emergency laparotomy for the hepatic injury was performed because of sustained hemodynamic instability after conservative therapy including high volumes of intravenous infusions and multiple transfusions. The patient's preoperative hemoglobin concentration was 6.4 mg/dL, and his hematocrit was 20%. The estimated blood loss during the operation was 7,000 mL, and total volume of intravenous infusions and transfusions was 8,000 mL. Postoperatively, the systemic hemodynamics were stabilized, and the right MCAFV and ICAFV increased to normal. The left MCAFV transiently increased to 80 cngsec before decreasing to normal; this was accompanied by a similar increase in the ipsilateral ICAFV (Figure 4). Monitoring the jugular bulb oxyhemoglobin saturation (Sjo2) was started postoperatively. The initial Sjo2 was 54.7%, which increased to a maximum of 82% during a 2-day interval before returning to normal. The ICP remained within the normal range. On the third hospital day, the patient gained consciousness, and no lesion was observed with serial cranial CT and magnetic resonance imaging (MRI). The patient was discharged with a mild residual memory disturbance 2 months after admission.
DISCUSSION The evaluation of cerebral hemodynamics in critically ill patients is difficult because of the short time allowed for measurements. With the development of TCD, serial evaluation of cerebral hemodynamics can be performed noninvasively, t,2 The practical usefulness of TCD monitoring has been well documented in situations such as severe head injury, 3,4 subarachnoid hemorrhage, 5 and the other cerebral vascular diseases. 6,7 However, there are few reports concerning the assessment of cerebral hemodynamics in patients with hypovolemic shock using TCD. We had the opportunity to evaluate the cerebral hemodynamics in a critically ill patient with hypovolemic shock caused by an abdominal injury. The initial results of TCD 587
588
AMERICAN JOURNAL OF EMERGENCY MEDICINE • Volume 15, Number 6 • October 1997
FIGURE 1. Cranial CT on admission showing no lesions.
examination showed a marked decrease in the MCAFVs, with an increase in their pulsatility indices. The diastolic flow signal of the left MCA was especially diminished, and its waveform appeared as a systolic peak. 8 In patients with head injuries, a characteristic progressive change in the TCD waveform can be seen during periods of increasing ICP. 4 The first change observed is a progressive decrease in the diastolic velocity. As the ICP approaches the diastolic pressure at the level of the microcirculation, the velocity approaches zero in end diastole, indicating that all of the forward flow is occurring during systole. With further increases in the ICR the waveform shows signs of cerebral circulatory arrest such as systolic spikes, to and fro, or no flow. 8 In an experimental study on the use of TCD in cases of increased ICR 9 the diastolic part of the flow velocity spectrum started to disappear once the diastolic perfusion pressure had decreased to a negative level, In this stage, only high systolic peaks are detectable. On the basis of the results from the initial TCD examination, we suspected the presence of intracranial hypertension caused by acute brain swelling or intracranial hemorrhage, and rapidly examined the ICP during the periods of preparing the operation. However, the ICP was normal, and the diastolic cerebral perfusion pressure was calculated to be 38 mm Hg. Hypocapnia can induce vasoconstriction, causing theoretical increase in the arterial blood pressure at which the MCAFV becomes zero in a pressure-velocity relationship. 1° However, blood gas analysis showed normocapnia. Therefore, these TCD findings showing nearly cerebral circulatory arrest were attributed to the hypovolemic shock. Jorgensen et al H reported changes in the middle cerebral artery velocity and pulsatility indice during induced hypovolemic shock in nine people. The hypovolemic shock was induced by passive head-up tilt. The 50 ° head-up tilt position was maintained for 60 minutes or until development of presyncopal symptoms. In all subjects, the middle cerebral artery velocity decreased and the pulsatility indice increased
FIGURE 2. (A) Chest CT on admission showing a pulmonary contusion and pneumothorax. (B) Abdominal CT shows a hematoma in the hepatic parenchyma (arrowheads) and a hemoperitoneum (arrows).
IIDA ET AL • CEREBRAL HEMODYNAMICS IN HYPOVOLEMIC SHOCK
during maintained head-up tilt. Eight of these subjects experienced presyncopal symptoms after 33 minutes in this state; this was associated with a mean arterial pressure of 65 mrn Hg (range, 32 to 84), decreased from 91 mm Hg (range, 87 to 102) at rest. The flow velocities decreased from a mean of 54 (32 to 62) to 25 (16 to 31) cm/sec, and the pulsatility indices increased from a mean of 0.8 (0.7 to 0.9) to 1.4 (1.1 to 2.5). In one subject, arterial collapse was observed when the diastolic velocity decreased to zero, corresponding to an arterial pressure at the level of the brain of 21 mm Hg. The systolic pressure was 47 rnm Hg, and mean arterial pressure in the brain was 34 mm Hg. Giller et a112 evaluated the cerebral hemodynamics of 13 healthy normotensive hypovolemic subjects during lower-body negative pressure. The middle cerebral artery flow velocity declined by 16% _+ 4% (mean + SD), and the ratio between TCD pulsatility and
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FIGURE 3. Transcranial Doppler sonographic spectral displays obtained on admission, showing decreased MCAFVs (right [A], 24 crrdsec; left [B], 10 cm/sec) and increased pulsatility indices (PIs: right [A], 2.21; left [B], 4.29). The diastolic flow signal of the left MCA was especially diminished, although the cerebral perfusion pressure was 51 mm Hg.
FIGURE 4. Changes in MCAFV in cm/sec (0), ICAFV in crrdsec (O), Sjo2 in % (IS]), and ICP in mm Hg (A). The left MCAFV transiently increased to 80 cm/sec before returning to normal; this was accompanied by a similar increase in the ipsilateral ICAFV. The value of Sjo2 also showed transient increase during a 2-day period postoperatively, followed by a return to normal. The ICP remained within the normal range.
systemic pulsatility increased 22% + 8%. These findings suggest a possibility of a decrease in cerebral blood flow that can cause neurological deficits during hypovolemia even in patients who maintain normal blood pressures. In the present case, the appearance of the systolic peak on TCD could not have been caused by a compromised cerebral perfusion pressure alone, and also may have been secondary to severe hypovolemia. The TCD and Sjo2 findings showed a postischemic hyperemia 2 days postoperatively. The initial postoperative Sjo2 value was 54.7%, and may have been less preoperatively. Generally, a Sjo2 of less than 50% is associated with cerebral hypoxia. 13 Therefore, the patient must have suffered from cerebral ischemia more than what was caused by the cerebral perfusion pressure alone, causing a residual memory disturbance. In conclusion, hypovolemia aggravates a reduced cerebral blood flow caused by a compromised cerebral perfusion pressure, and the TCD waveforms in patients with hypovolemic shock should be differentiated from those associated with intracranial hypertension.
REFERENCES 1. Aaslid R, Markwalder TM, Nernes H: Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982;57:769-774 2. Aaslid R: Transcranial Doppler Sonography. New York, NY, Springer-Verlag, 1986 3. Chan KH, Miller JD, Dearden NM, et al: The effect of changes in cerebral perfusion pressure upon middle cerebral artery blood flow velocity and jugular bulb venous oxygen saturation after severe brain injury. J Neurosurg 1992;77:55-61 4. Newell DW, Seller RW, Aaslid R: Head injury and cerebral circulatory arrest. In Newell DW, Aaslid R (eds): Transcranial Doppler. New York, NY, Raven, 1992, pp 109-121 5. Seiler RW, Newell DW: Subarachnoid hemorrhage and vase-
590
AMERICAN JOURNAL OF EMERGENCY MEDICINE • Volume 15, Number 6 • October 1997
spasm. In Newell DW, Aaslid R (eds): Transcranial Doppler. New York, NY, Raven, 1992, pp 101-108 6. Harders A, Bien S, Eggert HR, et al: Hemodynamic changes in arteriovenous malformations induced by superselective embolization: transcranial Doppler investigation. Neurol Res 1988; 10:239-245 7. Gomez CR, Gomez SM, Yoon KWP, et al: Evaluation and follow-up of carotid-cavernous fistulas by transcranial Doppler sonography: illustrative case. Neurosurgery 1989;24:749-753 8. Hassler W, Steinmetz H, Pirschel J: Transcranial Doppler study of intracranial circulatory arrest, J Neurosurg 1989;71:195-201 9. Takaya M, Moritake K, Fukuma A, et al: An experimental study on the transcranial Doppler ultrasonography in raised intracranial pressure. In Oka M, von Reutern GM, Furuhata H, et al: (eds):
Recent Advances in Neurosonology. Amsterdam, Excerpta Medica, 1992, pp 233-237 10. Aaslid R: Cerebral hemodynamics. In Newell DW, Aaslid R (eds): Transcranial Doppler. New York, NY, Raven, 1992, pp 49-55 11. Jorgensen LG, Perko M, Perko G, et al: Middle cerebral artery velocity during head-up tilt induced hypovolaemic shock in humans. Clin Physiol 1993; 13:323-326 12. Giller CA, Levine BD, Meyer Y, et al: The cerebral hemodynamics of normotensive hypovolemia during lower-body negative pressure. J Neurosurg 1992;75:961-966 13. Cruz J: Continuous versus serial global cerebral hemometabolic monitoring: applications in acute brain trauma. Acta Neurochir Suppl (Wien) 1988;42:35-39