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Neuronal activity alters local blood flow in brain tumour adjacent to the activating cortex
  1. KAORU SAKATANI,
  2. HUANCONG ZUO,
  3. YENG WANG
  1. Department of Neurosurgery, China-Japan Friendship Hospital, Beijing, China
  2. Group of Detection and Analysis of Human Body Movement, Program of BME, Department of Electrical Engineering, Tsinghua University, Japan
  3. Department of Rehabilitation, Takahashi Neurosurgical Hospital, Japan
  1. Dr Kaoru Sakatani, Department of Neurosurgery, China-Japan Friendship Hospital, Yinghua East Rd., Hepingli, Beijing 100029, People’s Republic of China. Telephone (fax) 0086 10 64203246; email sakatani{at}public.east.cn.net
  1. WEMARA LICHTY
  1. Department of Neurosurgery, China-Japan Friendship Hospital, Beijing, China
  2. Group of Detection and Analysis of Human Body Movement, Program of BME, Department of Electrical Engineering, Tsinghua University, Japan
  3. Department of Rehabilitation, Takahashi Neurosurgical Hospital, Japan
  1. Dr Kaoru Sakatani, Department of Neurosurgery, China-Japan Friendship Hospital, Yinghua East Rd., Hepingli, Beijing 100029, People’s Republic of China. Telephone (fax) 0086 10 64203246; email sakatani{at}public.east.cn.net
  1. KIYOMI YABU
  1. Department of Neurosurgery, China-Japan Friendship Hospital, Beijing, China
  2. Group of Detection and Analysis of Human Body Movement, Program of BME, Department of Electrical Engineering, Tsinghua University, Japan
  3. Department of Rehabilitation, Takahashi Neurosurgical Hospital, Japan
  1. Dr Kaoru Sakatani, Department of Neurosurgery, China-Japan Friendship Hospital, Yinghua East Rd., Hepingli, Beijing 100029, People’s Republic of China. Telephone (fax) 0086 10 64203246; email sakatani{at}public.east.cn.net

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Characteristics of blood flow in brain tumours have been studied extensively1; these studies are important for diagnosis of malignancy and therapy monitoring. Our study is the first to consider how activity dependent changes of regional cerebral blood flow (rCBF) alter tumour blood flow in the brain tumour adjacent to the activating cortex. Such an interaction between cortical blood flow and tumour blood flow may be of value for evaluating mechanisms of neurological symptoms associated with brain tumours.

Neuronal activation causes an increase of regional cerebral blood flow (rCBF) in the activating cortical area.2 Near infrared spectroscopy (NIRS) demonstrates the increase in rCBF during neuronal activity as increases in oxygenated haemoglobin (oxy-Hb) and total haemoglobin (total-Hb) with a decrease in deoxyhaemoglobin (deoxy-Hb)3-5; NIRS is an optical method to measure concentration changes of oxy-Hb, deoxy-Hb, and total-Hb (oxy-Hb+deoxy-Hb) in cerebral vessels by means of the characteristic absorption spectra of haemoglobin in the near infrared range.

In the present study, we measured changes of oxygenation and haemodynamics in the brain tumour adjacent to the activating cortex by means of NIRS. We found transient decreases in oxy-Hb and total-Hb in the tumour during neuronal activation, suggesting that the local blood flow of the tumour was decreased by a transient increase of rCBF induced by neuronal activation.

The patient was a 35 year old right handed man who presented with complaints of headache and dizziness. A neurological examination showed no abnormalities and a decline in language functions. A postcontrast CT showed a well defined large enhancing tumour (4×5 cm) compressing the left frontal lobe. Computed tomographic angiography showed that the branches of the left middle cerebral artery supplied the tumour (figure A). The patient underwent a left frontal craniotomy for removal of the tumour; the pathological diagnosis was meningioma. The NIRS measurement was performed before the operation.

(A) CT angiography of the brain tumour. Note that the tumour was supplied by the branches of the left middle cerebral artery. (B) Oxygenation changes in the brain tumour during the naming task measured by NIRS. The ordinates indicate concentration changes of oxy-Hb, deoxy-Hb, and total-Hb in arbitrary units (au). Horizontal thick bar indicates the period of the task.

We measured haemodynamic changes in the brain tumour during neuronal activation in the left frontal lobe induced by cognitive tasks. We monitored concentration changes of oxy-Hb, deoxy-Hb, and total-Hb, using an NIRO-500 instrument (Hamamatsu Photonics KK, Japan). The optodes were placed at an interoptode distance of 3.5 cm on the left forehead so that the centre of the two optodes was placed on the centre of the tumour. With an optode distance of 4 cm, correlations of oxy-Hb and total-Hb measured by NIRS and rCBF measured by PET suggested that the reliable penetration depth of near infrared light into brain tissue is about 1.3 cm3; thus the present NIRS measurement area was restricted in the tumour. The patient was seated and had his eyes open during the NIRS measurement. Informed consent was obtained from the patient.

To activate the left frontal lobe, we used the following four tasks: (1) semantic verbal fluency, which entails naming as many items in a semantic category (for example, animals) as possible; (2) confrontational naming, which involves naming ordinary items presented by the tester; (3) backward digit span, a working memory task which involves reporting of digits (2 to 8) in the reverse order; (4) reading, which entails reading a short descriptive passage aloud. The speech responses of the patient to the tasks were normal.

Figure B shows an example of changes in NIRS during the naming task. After the beginning of the task, oxy-Hb and total-Hb decreased to negative values during the task, and deoxy-Hb also decreased. These changes returned to the control level gradually after the end of the task. The other tasks also caused similar changes of oxy-Hb, total-Hb, and deoxy-Hb.

The rCBF in the left frontal lobe is generally increased by all the tasks used in the present study.3-5 Indeed, our NIRS activation study using the cognitive tasks showed increases in oxy-Hb and total-Hb in the left frontal lobe in most normal adults—for example, increases in oxy-Hb and total-Hb— were found in 92.3% of young adult subjects (mean (SD) 28.8 (4.4) years) during the word fluency task (unpublished data). Therefore, although we could not measure the changes in rCBF in the left frontal lobe of the patient, the evidence from our previous studies strongly suggests that the tasks caused an increase in rCBF in the left frontal lobe of the patient.

The decrease in oxy-Hb and total-Hb recorded from the brain tumour indicates a decrease of local blood flow in the tumour because the NIRS measurement area was restricted to the brain tumour.3 The decreases in oxy-Hb and total-Hb were found only during the tasks; consequently, these changes were probably not due to changes in systemic blood pressure, which can alter tumour blood flow.1 Based on these assumptions, we suggest that the increase of rCBF in the left frontal lobe induced by the tasks stole the local blood flow of the brain tumour through the cortical branches, leading to the decrease of local blood flow in the tumour.

The present report suggests that activity dependent increase in rCBF can steal blood flow from the adjacent tissues including non-activating cortex. Recent NIRS activation studies have shown that cognitive tasks cause decreases in oxy-Hb and total-Hb in the left frontal lobe in some normal subjects4 5; these decreases indicate a decrease in rCBF.5 Although the physiological mechanisms of the decrease in rCBF during neuronal activity have not yet been elucidated, we hypothesise that a stealing of blood flow is one of the mechanisms.4 The present report supports this hypothesis.

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