J Neurosurg 50:483-488, 1979
Cerebral hemodynamic changes during plateau waves in brain-tumor patients MASAYUKI MATSUDA, M.D., SHUNICHI YONEDA, M.D., HAJIME HANDA, M.D., AND HIROSHI GOTOH, M.D.
Department of Neurosurgery, Kyoto University Medical School, Kyoto, Japan t~ The plateau wave, one of the wave forms observed in patients with increased intracranial pressure, has previously been extensively investigated, but its pathophysiological aspect is as yet unclear. The authors undertook a study of cerebral hemodynamic changes while the plateau waves were observed in five brain-tumor patients. Although the number of cases studied was small, a remarkable decrease in cerebrovascular resistance was seen in all patients during the plateau waves. It is suggested that the plateau waves are caused by a marked cerebral vasodilatation. The present results support the thesis that cerebral blood volume is increased during the plateau waves. The plateau waves are closely related to the intrinsic vasomotor control of cerebral circulation, and can occur as long as cerebral vasodilating ability is maintained, irrespective of the existence of cerebral autoregulation. KEY WORDS brain tumor
9
intracranial pressure
T
HE relationship between cerebral blood flow (CBF) and intracranial pressure (ICP) has been studied extensively both clinically8,e,9,1a,26,27,a~ and experimentally. 7,a,14'xS,2~ It is well known that the patients with brain tumors sometimes have paroxysmal symptoms such as severe headaches and vomiting, accompanied by an acute temporary increase in ICP. This intermittent marked increase in ICP was named "plateau wave" by Lundberg. ~6 Plateau waves have been reported in various neurosurgical cases TM including brain t u m o r , 1'2'19'26'27'31'35'43 head injury, 3,4,39 benign intracranial hypertension, TM hydrocephalus, 31,37 and subarachnoid hemorrhage? TM They are observed mostly in brain-tumor patients with a fairly advanced degree of intracranial hypertension. 27 These patients are usually alert during the plateau waves in spite of the severity of their intracranial condition with a marked reduction of cerebral perfusion pressure, s~ The plateau waves seen clinically have no counterpart in experimental observations. TM We have recorded both CBF and ICP simultaneously during the plateau waves in five braintumor patients and have attempted to analyze the accompanying cerebral hemodynamic changes with a review of the literature.
J. Neurosurg. / Volume 50 / April, 1979
9 plateau wave
9 cerebral hemodynamic change
9
Clinical Materials and Methods
Five patients, three males and two females, with supratentorial tumors were studied. Histology was either glioblastoma multiforme or astrocytoma. Their ages ranged from 29 to 52 years. The ICP was measured as epidural pressure (EDP) with the use of the semiconductor film strain transducer* (SFT), 44 which was attached to the dural surface through a burr hole made at the coronal suture 3 to 4 cm from the midline on the side opposite to the tumor. The ICP was recorded continuously,t and the regional cerebral blood flow (rCBF) was measured by the 188Xe clearance method. The scinticamera$ with a 4000-hole collimator was placed over the hemisphere on the other side of the tumor. The validity of the use of the scinticamera for rCBF study was reported in the
*SFT transducer manufactured by Matsushita Electric Industrial Co., Ltd., Central Research Laboratory, Kadoma, Osaka 571, Japan. tType 3047 Recorder manufactured by Yokogawa Electric Works, Ltd., Chuo Ku, Tokyo 104, Japan. :~Pho/Gamma III scinticamera manufactured by Nuclear Chicago Co., Des Plaines, Illinois. 483
M. Matsuda, S. Yoneda, H. Handa and H. Gotoh
Fic. 1. Case 3. Simultaneous recording of epidural pressure (EDP) and blood pressure (BP) in a patient with glioblastoma. Arrow indicates intracarotid injection of lSsXe.
literature. 1~176Approximately 5 mCi of laaXe dissolved in 2 ml of saline was injected into the internal carotid artery through a polyethylene catheter. The rCBF was measured in eight regions and calculated by a computerw connected to the scinticamera. The initial slope index83 was used for measuring CBF because of the short duration of the plateau waves. The brainblood partition coefficient of gray matter was corrected according to the hemoglobin content. 11 Blood pressure was monitored with the use of the SFT transducer which was connected to a polyethylene catheter in the internal carotid artery or radial artery, and recorded simultaneously with ICP. Mean arterial blood pressure (MABP) was calculated by adding onethird of the pulse pressure to the diastolic pressure. The ICP was calculated in the same way and expressed as mean pressure. Cerebral perfusion pressure (CPP) and cerebrovascular resistance (CVR) were derived from the following formulas: CPP = MABP - ICP, CVR = CPP/CBF. Arterial blood gas was analyzed by a blood gas analyzer. II All procedures were performed under local anesthesia. Atropin sulfate, 0.5 mg, was given intramuscularly before the procedure.
w 200 computer manufactured by Shimadzu Seisakusho, Ltd., Nakagyo Ku, Kyoto 604, Japan. I]ABL 1 blood gas analyzer manufactured by Radiometer A/S, 72 Emdrupvej, DK 2400, Copenhagen, Denmark. 484
Results
The data for the five patients are shown in Table 1. The simultaneous recordings of ICP and blood pressure in Cases 3, 4, and 5 are illustrated in Figs. 1-3. All the patients but Case 5 were alert and cooperative throughout the study. They all complained of headache while the plateau waves were being observed, but the fifth patient was somnolent. His control ICP and MABP were 84 mm Hg and 118.3 mm Hg, respectively, which brought CPP down to 34.3 mm Hg. During the plateau wave, ICP rose to 123.3 mm Hg, and CPP further decreased to 16.7 mm Hg. The CBF of this patient was accordingly very low, but did not show any significant difference between control values and values during the plateau wave, 19.5 and 21.5 ml/100 gm/min, respectively. The CVR showed a marked decrease by 55.7% from 1.76 to 0.78 mm Hg/(ml/100 gm/min). In the other four patients (Cases 1, 2, 3, and 4), control ICP ranged from 16.0 to 30.7 mm Hg, with CPP of 62.3 to 94.4 mm Hg. During the plateau waves, the ICP increased to between 50.0 and 80.0 mm Hg, and CPP decreased to between 26.6 and 66.0 mm Hg. The remarkable decrease in CPP caused CBF to decrease by 19.3% in Case 2 and 27.5% in Case 3. The accompanying decrease in PaCO2, particularly in Case 3, might have had some effect on the decrease in CBF. The CBF in Case 1 was decreased by 15.1% and that in Case 4 did not change. The CVR decreased in all cases by 14.4% to 49.1%. J. Neurosurg. / Volume 50 / April, 1979
Plateau waves and cerebral hemodynamic changes
FIG. 2. Case 4. Simultaneous recordings of epidural pressure (EDP) and blood pressure (BP) in a patient with astrocytoma. Arrow indicates intracarotid injection of lSSXe.
Discussion The EDP as recorded here might not be equivalent to ICP in the strict sense, since EDP, or surface brain pressure, is reported to be higher than cerebrospinal fluid (CSF) pressure or ventricular fluid pressure
(VFP)? 't6'36 However, in our experimental study on monkeys, EDP was found to be the same as VFP. 42 Also, we prefer the epidural device to ventricular cannulation because it reduces the risk of infection. The plateau waves are characterized by a height of 50 to 100 m m Hg and a duration of 5 to 20 minutes. 26 In this
FIG. 3. Case 5. Simultaneous recording of epidural pressure (EDP) and blood pressure (BP) in a patient with glioblastoma. Arrow indicates intracarotid injection of 13aXe. J. Neurosurg. / Volume 50 / April, 1979
485
M. Matsuda, S. Yoneda, H. Handa and H. Gotoh TABLE 1 Parameters measured in five patients*
Case No. 1 2 3 4 5
Age CBF (yrs), (ml/100gm/min) Sex C PW 42, M 29, M 31, F 49, F 52, M
43.6 33.6 38.5 44.5 19.5
37.0 27.1 27.9 42.9 21.5
MABP (ram Hg) C PW 121.3 120.7 86.3 78.3 118.3
118.7 118.7 88.3 96.0 140.0
ICP (mm Hg) C PW 30.7 26.3 21.3 16.0 84.0
52.7 80.0 61.7 50.0 123.3
CPP (mm Hg) C PW 90.6 94.4 65.0 62.3 34.3
66.0 38.7 26.6 46.0 16.7
CVRt C
PW
2.08 2.81 1,69 1.40 1.76
1.78 1.43 0.95 1.07 0.78
PaCO2 (ram Hg) C PW 40.7 43.5 32.5 34.2 29.9
39.0 41.6 27.5 32.7 30.8
*CBF = cerebral blood flow; MABP = mean arterial blood pressure; ICP = intracranial pressure; CPP = cerebral perfusion pressure; CVR = cerebrovascular resistance; PaCO2 = partial pressure of CO2 in arterial blood; C = control values; and PW = values during plateau waves. mm Hg tMeasured as ml/100 gin/rain"
study, all the plateau waves lasted less than 10 minutes, but they were long enough for CBF measurement (laSXe injection) by the initial-slope index method ?8 Kety, et al., TM found that CBF was significantly reduced in the brain-tumor patients with C S F pressures greater than 33 mm Hg. Greenfield and Tindall 6 reported a significant reduction of internal carotid blood flow at a CSF pressure of 28 mm Hg or above, and their patients remained asymptomatic until CSF pressure reached 68 mm Hg. Heilbrun, et al.,9 reported a remarkable decrease in CBF when ICP (EDP) reached 65 to 90 mm Hg and CPP decreased to 15 mm Hg. Lundberg, et al., 27 and P~lvSlgyW observed a reduction in rCBF in brain-tumor patients with increased ICP. The effect of increased ICP on CBF has been extensively investigated in animal experiments. The critical level of ICP that causes a reduction of CBF varies from 35 to 100 mm Hg, depending on the method of raising ICP. s,14,16,2~ As ICP affects CBF secondarily to changes in CPP, the effect of increased ICP on CBF should be investigated from the standpoint of CPP. 8,3~ The C P P is generally defined as the difference between MABP and ICP. s,ls,8~ The mechanism that maintains CBF during intracranial hypertension is equivalent to the process of CBF autoregulation that occurs during alterations in arterial pressure? The lower limit of CPP in CBF autoregulation is reported to be from 30 to 80 mm Hg in experimental animals. ~,saSag,3~ When a decrease in C P P is associated with an increase in ICP, maintenance of CBF becomes dependent on dilatation of the resistance vessels, that is, the decrease in CVR. Experimental reports have indicated a progressive fall in CVR and cerebrovascular dilatation in response to an increase in ICP. 14,15,~ Reports of cortical vasodilatation observed through a cranial window 4~ and vasodilatation seen on angiograms 27 support the concept of CVR decrease during intracranial 486
hypertension. The present results also showed that CVR decreased in every case during the plateau waves. The increased ICP created experimentally and the one observed during the plateau waves might be substantially different. The former is passive and the latter active and spontaneous; however, in either case, the CVR decreased. On the other hand, Kety, et al., TM concluded that CVR increased when ICP increased. This contradictory result might be explained by their calculations of CVR as MABP divided by CBF and the fact that ICP was not taken into account. Human studies showed a decrease in CBF ~7 and an increase in CBV 35 during the plateau waves. This discrepancy between CBF and CBV was explained by a shift of main CVR from the arterial to the venous side. ~8 In their experiments, Langfitt, et al., 22 and Grubb, et al.,7 reported an increase in CBV during increased ICP, while Lowell and Bloor ~5 reported a decrease. This decrease in CBV was attributed to loss of cerebral autoregulation. 7 The present study shows definitely that the plateau waves are accompanied or caused by a marked cerebral vasodilatation, and gives support to the report of CBV increase during the plateau waves, s5 However, what causes a marked cerebral vasodilatation is not yet known. Although it is one of the most potent cerebral vasodilators, CO~ is not likely to cause the plateau waves that appear and disappear abruptly in a matter of seconds, and, in this study, in the initial phase of the plateau waves PaCO~ was not increased at all. An increase in MABP observed during the plateau waves with CBF measurement in Cases 4 and 5 actually had occurred 15 to 20 minutes before the onset of the plateau waves. This MABP increase did not always accompany every plateau wave even in the same case, and this finding confirms the observation that the plateau waves occurred irrespective of variations of systemic blood pressure? e It is reported that the plateau waves are closely related to the intrinsic vasomotor control of J. Neurosurg. / Volume 50 / April, 1979
Plateau waves and cerebral hemodynamic changes cerebral circulation? 6a7,35 The m e c h a n i s m that can bring about a remarkable cerebral vasodilatation in a matter of seconds could be neurogenic. The plateau waves are observed in patients who are in an advanced stage of persistent intracranial hypertension with marked impairment of intracranial spatial compensation) 6a7 Many of the patients with brain tumor have disturbed autoregulation? T M The vasodilating ability was preserved in the patient in Case 5, who was in critical condition, with a very high ICP, and very low C P P and CBF. In conclusion, the plateau waves are caused by a marked cerebral vasodilatation and could occur as long as cerebral vasodilating ability is maintained, irrespective of the existence of cerebral autoregulation.
11.
12.
13.
14.
Acknowledgments
The authors are grateful to Mr. Tohru Fujita and Mr. Takao Mukai for their assistance in CBF measurements.
15.
References
1. Becker DP, Young HF, Vries JK, et al: Pre, intra and post-operative cerebral perfusion pressure monitoring of patients with brain tumors: prevention ofischemic insults, in Lundberg N, Pont6n U, Brock M (eds): Intracraniai Pressure II. Berlin~Heidelberg~New York: Springer-Verlag, 1975, pp 503-507 2. Brock M, Zillig C, Wiegand H, et al: The influence of dexamethasone therapy in ICP in patients with tumors of the posterior fossa, in Beks JWF, Bosch DA, Brock M (eds): Intracranial Pressure IlL Berlin~Heidelberg~ New York: Springer-Verlag, 1976, pp 236-246 3. Bruce DA, Langfitt TW, Miller JD, et al: Regional cerebral blood flow, intracranial pressure, and brain metabolism in comatose patients. J Neurosurg 38:131-144, 1973 4. C611ice M, Rossanda M, Beduschi A, et al: Management of head injury by means of ventricular fluid pressure monitoring, in Beks JWF, Bosch DA, Brock M (eds): lntracranial Pressure lIl. Berlin~Heidelberg~New York: Springer-Verlag, 1976, pp 101-109 5. Gobiet W, Back W J, Liesegang J, et al: Long-time monitoring of epidural pressure in man, in Brock M, Dietz H (eds): Intracraniai Pressure. Experimental and Clinical Aspects. Berlin/Heidelberg/New York: Springer-Verlag, 1972, pp 14-17 6. Greenfield JC Jr, Tindall GT: Effect of acute increase in intracranial pressure on blood flow in the internal carotid artery of man. J Clin Invest 44:1343-1351, 1965 7. Grubb RL Jr, Raichle ME, Phelps ME, et al: Effects of increased intracranial pressure on cerebral blood volume, blood flow, and oxygen utilization in monkeys. J Neurosurg 43:385-398, 1975 8. H~iggendal E, LSfgren J, Nilsson N J, et al: Effects of varied cerebrospinal fluid pressure on cerebral blood flow in dogs. Acta Physiol Scand 79:262-271, 1970 9. Heilbrun MP, Jorgensen PB, Boysen G: Relationships between cerebral perfusion pressure and regional cerebral blood flow in patients with severe neurological disorders. Stroke 3:181-195, 1972 10. Heiss W-D, Prosenz P, Roszuczky A: Technical considerations in the use of a gamma camera 1,600-channel
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18. 19.
20. 21. 22.
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25.
analyzer system for the measurement of regional cerebral blood flow. J Nucl Med 13:534-543, 1972 HCedt-Rasmussen K, Sveinsdottir E, Lassen NA: Regional cerebral blood flow in man determined by intra-arterial injection of radioactive inert gas. Circ Res 18:237-247, 1966 Johnston I, Paterson A: Intracranial pressure monitoring in patients with benign intracranial hypertension, in Lundberg N, Pont6n U, Brock M (eds): lntraeranial Pressure II. Berlin/Heidelberg/New York: SpringerVerlag, 1975, pp 500-502 Johnston IH, Rowan JO: Raised intracranial pressure and cerebral blood flow. 3. Venous outflow tract pressures and vascular resistances in experimental intracranial hypertension. J Neural Neurosurg Psychiatry 37:392-402, 1974 Johnston IH, Rowan JO, Harper AM, et al: Raised intracranial pressure and cerebral blood flow. 1. Cisterna magna infusion in primates. J Neural Neurosurg Psychiatry 35:285-296, 1972 Johnston IH, Rowan JO, Harper AM, et al: Raised intracranial pressure and cerebral blood flow. 2. Supratentorial and infratentorial mass lesions in primates. J Neural Neurosurg Psychiatry 36:161-170, 1973 JCrgensen PB, Riishede J: Comparative clinical studies of epidural and ventricular pressure, in Brock M, Dietz H (eds): Intracranial Pressure. Experimental and Clinical Aspects. Berlin/Heidelberg/New York: Springer-Verlag, 1972, pp 41-45 Kassell NF, Peerless SJ, Reilly PL: ICP, aneurysms, and subarachnoid hemorrhage, in Beks JWF, Bosch DA, Brock M (eds): Intracranial Pressure III. Berlin/Heidelberg/New York: Springer-Verlag, 1976, pp 147-151 Kety SS, Shenkin HA, Schmidt CF: The effects of increased intracranial pressure on cerebral circulatory functions in man. J Clin Invest 27:493-499, 1948 Kullberg G, SundNirg G: Reduction of raised intracranial pressure following infusion of mannitol. A review of clinical pressure recordings, in Beks JWF, Bosch DA, Brock M (eds): Intracranial Pressure III. Berlin/Heidelberg/New York: Springer-Verlag, 1976, pp 224-230 Langfitt TW, Kassell NF, Weinstein JD: Cerebral blood flow with intracranial hypertension. Neurology 15:761-773, 1965 Langfitt TW, Weinstein JD, Kassell NF: Cerebral vasomotor paralysis produced by intracranial hypertension. Neurology 15:622-641, 1965 Langfitt TW, Weinstein JD, Sklar FH, et al: Contribution of intracranial blood volume to three forms of experimental brain swelling. Johns Hopkins Med J 122:261-270, 1968 Lewis HP, McLaurin RL: Regional cerebral blood flow and increased intracranial pressure produced by simulated hydrocephalus, mass lesion, and cerebral edema. Surg Forum 22:424-426, 1971 Lorenz R: The Cushing response, in Beks JWF, Bosch DA, Brock M (eds): Intracranial Pressure III. Berlin/Heidelberg/New York: Springer-Verlag, 1976, pp 270-278 Lowell HM, Bloor BM: The effect of increased intracranial pressure on cerebrovascular hemodynamics. J Neurosurg 34:760-769, 1971 487
M. Matsuda, S. Yoneda, H. Handa and H. Gotoh 26. Lundberg N: Continuous recording and control of ventricular fluid pressure in neurosurgical practice. Aeta Psychiatr Stand 36 (Suppl 149):1-193, 1960 27. Lundberg N, Cronqvist S, Kj~Ulquist /~: Clinical investigations on interrelations between intracranial pressure and intracranial hemodynamics. Prog Brain Res 30:69-75, 1968 28. Lundberg N, Kj~illquist It, Kullberg G, et al: Nonoperative management of intracranial hypertension, in Krayenbfihl H, et al (eds): Advances and Technical Standards in Neurosurgery, Vol 1. Wien/New York: Springer-Verlag, 1974, pp 3-59 29. Miller JD, Stanek AE, Langfitt TW: Cerebral blood flow regulation during experimental brain compression. J Neurosurg 39:186-196, 1973 30. Miller JD, Stanek AE, Langfitt TW: Concepts of cerebral perfusion pressure and vascular compression during intracranial hypertension. Prog Brain Res 35:411-432, 1972 31. Nornes H, Magnaes B, Aaslid R: Observations in intracranial pressure plateau waves, in Lundberg N, Pont6n U, Brock M (eds): Intraeranial Pressure II. Berlin/Heidelberg/New York: Springer-Verlag, 1975, pp 421-426 32. PfilvSlgyi R: Regional cerebral blood flow in patients with intracranial tumors. J Neurosurg 31:149-163, 1969 33. Paulson OB, Cronqvist S, Risberg J, et al: Regional cerebral blood flow: A comparison of 8-detector and 16detector instrumentation. J Nucl Med 10:164-173, 1969 34. Paulson OB, Olesen J, Christensen MS: Restoration of autoregulation of cerebral blood flow by hypocapnia. Neurology 22:286-293, 1972 35. Risberg J, Lundberg N, Ingvar DH: Regional cerebral blood volume during acute transient rises of the intracranial pressure (plateau waves). J Neurosurg 31: 303-310, 1969 36. Sundb~irg G, Nornes H: Simultaneous recording of the epidural and ventricular fluid pressure, in Brock M, Dietz H (eds): Intracranial Pressure. Experimental and
488
Aspects. Berlin/Heidelberg/New York: Springer-Verlag, 1972, pp 46-50 37. Symon L, Dorsch NWC: Use of long-term intracranial pressure measurement to assess hydrocephalic patients prior to shunt surgery. J Nenrosurg 42:258-273, 1975 38. Symon L, Pasztor E, Branston NM, et al: Effect of supratentorial space-occupying lesions on regional intracranial pressure and local cerebral blood flow: an experimental study in baboons. J Neurol Neurosurg Psychiatry 37:617-626, 1974 39. Tindall GT, McGraw CP, Iwata K: Subdural pressure monitoring in head-injured patients, in Brock M, Dietz Clinical
H (eds): Intracranial Pressure. Experimental and Clinical Aspects. Berlin/Heidelberg/New York:
Springer-Verlag, 1972, pp 9-13 40. Torizuka K, Hamamoto K, Morita R, et al: Regional cerebral blood flow measurement with xenon-133 and the scinticamera. Am J Roentgenol Radium Ther Nucl Med 112:691-700, 1971 41. Weinstein JD, Langfitt TW: Responses of cortical vessels to brain compression: Observations through a transparent calvarium. Surg Forum 18:430-432, 1967 42. Yoneda S, Gotoh H, Matsuda M, et al: Increased intracranial pressure and tentorial shear strain. Neurol Med Chit (In press) 43. Yoneda S, Matsuda M, Goto H, et al: [The effects of glycerol and mannitol on the epidural intracranial pressure of the patients with increased intracranial pressure.] Arch Jpn Chir 46:731-739, 1977 (Jpn) 44. Yoneda S, Matsuda M, Shimizu Y, et al: SFT - - A new device for continuous measurement of intracranial pressure. Surg Neurol 1:13-15, 1973
Address reprint requests to: Masayuki Matsuda, M.D., Department of Neurosurgery, Kyoto University Medical School, 54 Kawahara Cho, Shogoin, Sakyo Ku, Kyoto 606, Japan.
J. Neurosurg. / Volume 50 / April, 1979
Cerebral hemodynamic changes during plateau waves in brain-tumor patients MASAYUKI MATSUDA, M.D., SHUNICHI YONEDA, M.D., HAJIME HANDA, M.D., AND HIROSHI GOTOH, M.D.
Department of Neurosurgery, Kyoto University Medical School, Kyoto, Japan t~ The plateau wave, one of the wave forms observed in patients with increased intracranial pressure, has previously been extensively investigated, but its pathophysiological aspect is as yet unclear. The authors undertook a study of cerebral hemodynamic changes while the plateau waves were observed in five brain-tumor patients. Although the number of cases studied was small, a remarkable decrease in cerebrovascular resistance was seen in all patients during the plateau waves. It is suggested that the plateau waves are caused by a marked cerebral vasodilatation. The present results support the thesis that cerebral blood volume is increased during the plateau waves. The plateau waves are closely related to the intrinsic vasomotor control of cerebral circulation, and can occur as long as cerebral vasodilating ability is maintained, irrespective of the existence of cerebral autoregulation. KEY WORDS brain tumor
9
intracranial pressure
T
HE relationship between cerebral blood flow (CBF) and intracranial pressure (ICP) has been studied extensively both clinically8,e,9,1a,26,27,a~ and experimentally. 7,a,14'xS,2~ It is well known that the patients with brain tumors sometimes have paroxysmal symptoms such as severe headaches and vomiting, accompanied by an acute temporary increase in ICP. This intermittent marked increase in ICP was named "plateau wave" by Lundberg. ~6 Plateau waves have been reported in various neurosurgical cases TM including brain t u m o r , 1'2'19'26'27'31'35'43 head injury, 3,4,39 benign intracranial hypertension, TM hydrocephalus, 31,37 and subarachnoid hemorrhage? TM They are observed mostly in brain-tumor patients with a fairly advanced degree of intracranial hypertension. 27 These patients are usually alert during the plateau waves in spite of the severity of their intracranial condition with a marked reduction of cerebral perfusion pressure, s~ The plateau waves seen clinically have no counterpart in experimental observations. TM We have recorded both CBF and ICP simultaneously during the plateau waves in five braintumor patients and have attempted to analyze the accompanying cerebral hemodynamic changes with a review of the literature.
J. Neurosurg. / Volume 50 / April, 1979
9 plateau wave
9 cerebral hemodynamic change
9
Clinical Materials and Methods
Five patients, three males and two females, with supratentorial tumors were studied. Histology was either glioblastoma multiforme or astrocytoma. Their ages ranged from 29 to 52 years. The ICP was measured as epidural pressure (EDP) with the use of the semiconductor film strain transducer* (SFT), 44 which was attached to the dural surface through a burr hole made at the coronal suture 3 to 4 cm from the midline on the side opposite to the tumor. The ICP was recorded continuously,t and the regional cerebral blood flow (rCBF) was measured by the 188Xe clearance method. The scinticamera$ with a 4000-hole collimator was placed over the hemisphere on the other side of the tumor. The validity of the use of the scinticamera for rCBF study was reported in the
*SFT transducer manufactured by Matsushita Electric Industrial Co., Ltd., Central Research Laboratory, Kadoma, Osaka 571, Japan. tType 3047 Recorder manufactured by Yokogawa Electric Works, Ltd., Chuo Ku, Tokyo 104, Japan. :~Pho/Gamma III scinticamera manufactured by Nuclear Chicago Co., Des Plaines, Illinois. 483
M. Matsuda, S. Yoneda, H. Handa and H. Gotoh
Fic. 1. Case 3. Simultaneous recording of epidural pressure (EDP) and blood pressure (BP) in a patient with glioblastoma. Arrow indicates intracarotid injection of lSsXe.
literature. 1~176Approximately 5 mCi of laaXe dissolved in 2 ml of saline was injected into the internal carotid artery through a polyethylene catheter. The rCBF was measured in eight regions and calculated by a computerw connected to the scinticamera. The initial slope index83 was used for measuring CBF because of the short duration of the plateau waves. The brainblood partition coefficient of gray matter was corrected according to the hemoglobin content. 11 Blood pressure was monitored with the use of the SFT transducer which was connected to a polyethylene catheter in the internal carotid artery or radial artery, and recorded simultaneously with ICP. Mean arterial blood pressure (MABP) was calculated by adding onethird of the pulse pressure to the diastolic pressure. The ICP was calculated in the same way and expressed as mean pressure. Cerebral perfusion pressure (CPP) and cerebrovascular resistance (CVR) were derived from the following formulas: CPP = MABP - ICP, CVR = CPP/CBF. Arterial blood gas was analyzed by a blood gas analyzer. II All procedures were performed under local anesthesia. Atropin sulfate, 0.5 mg, was given intramuscularly before the procedure.
w 200 computer manufactured by Shimadzu Seisakusho, Ltd., Nakagyo Ku, Kyoto 604, Japan. I]ABL 1 blood gas analyzer manufactured by Radiometer A/S, 72 Emdrupvej, DK 2400, Copenhagen, Denmark. 484
Results
The data for the five patients are shown in Table 1. The simultaneous recordings of ICP and blood pressure in Cases 3, 4, and 5 are illustrated in Figs. 1-3. All the patients but Case 5 were alert and cooperative throughout the study. They all complained of headache while the plateau waves were being observed, but the fifth patient was somnolent. His control ICP and MABP were 84 mm Hg and 118.3 mm Hg, respectively, which brought CPP down to 34.3 mm Hg. During the plateau wave, ICP rose to 123.3 mm Hg, and CPP further decreased to 16.7 mm Hg. The CBF of this patient was accordingly very low, but did not show any significant difference between control values and values during the plateau wave, 19.5 and 21.5 ml/100 gm/min, respectively. The CVR showed a marked decrease by 55.7% from 1.76 to 0.78 mm Hg/(ml/100 gm/min). In the other four patients (Cases 1, 2, 3, and 4), control ICP ranged from 16.0 to 30.7 mm Hg, with CPP of 62.3 to 94.4 mm Hg. During the plateau waves, the ICP increased to between 50.0 and 80.0 mm Hg, and CPP decreased to between 26.6 and 66.0 mm Hg. The remarkable decrease in CPP caused CBF to decrease by 19.3% in Case 2 and 27.5% in Case 3. The accompanying decrease in PaCO2, particularly in Case 3, might have had some effect on the decrease in CBF. The CBF in Case 1 was decreased by 15.1% and that in Case 4 did not change. The CVR decreased in all cases by 14.4% to 49.1%. J. Neurosurg. / Volume 50 / April, 1979
Plateau waves and cerebral hemodynamic changes
FIG. 2. Case 4. Simultaneous recordings of epidural pressure (EDP) and blood pressure (BP) in a patient with astrocytoma. Arrow indicates intracarotid injection of lSSXe.
Discussion The EDP as recorded here might not be equivalent to ICP in the strict sense, since EDP, or surface brain pressure, is reported to be higher than cerebrospinal fluid (CSF) pressure or ventricular fluid pressure
(VFP)? 't6'36 However, in our experimental study on monkeys, EDP was found to be the same as VFP. 42 Also, we prefer the epidural device to ventricular cannulation because it reduces the risk of infection. The plateau waves are characterized by a height of 50 to 100 m m Hg and a duration of 5 to 20 minutes. 26 In this
FIG. 3. Case 5. Simultaneous recording of epidural pressure (EDP) and blood pressure (BP) in a patient with glioblastoma. Arrow indicates intracarotid injection of 13aXe. J. Neurosurg. / Volume 50 / April, 1979
485
M. Matsuda, S. Yoneda, H. Handa and H. Gotoh TABLE 1 Parameters measured in five patients*
Case No. 1 2 3 4 5
Age CBF (yrs), (ml/100gm/min) Sex C PW 42, M 29, M 31, F 49, F 52, M
43.6 33.6 38.5 44.5 19.5
37.0 27.1 27.9 42.9 21.5
MABP (ram Hg) C PW 121.3 120.7 86.3 78.3 118.3
118.7 118.7 88.3 96.0 140.0
ICP (mm Hg) C PW 30.7 26.3 21.3 16.0 84.0
52.7 80.0 61.7 50.0 123.3
CPP (mm Hg) C PW 90.6 94.4 65.0 62.3 34.3
66.0 38.7 26.6 46.0 16.7
CVRt C
PW
2.08 2.81 1,69 1.40 1.76
1.78 1.43 0.95 1.07 0.78
PaCO2 (ram Hg) C PW 40.7 43.5 32.5 34.2 29.9
39.0 41.6 27.5 32.7 30.8
*CBF = cerebral blood flow; MABP = mean arterial blood pressure; ICP = intracranial pressure; CPP = cerebral perfusion pressure; CVR = cerebrovascular resistance; PaCO2 = partial pressure of CO2 in arterial blood; C = control values; and PW = values during plateau waves. mm Hg tMeasured as ml/100 gin/rain"
study, all the plateau waves lasted less than 10 minutes, but they were long enough for CBF measurement (laSXe injection) by the initial-slope index method ?8 Kety, et al., TM found that CBF was significantly reduced in the brain-tumor patients with C S F pressures greater than 33 mm Hg. Greenfield and Tindall 6 reported a significant reduction of internal carotid blood flow at a CSF pressure of 28 mm Hg or above, and their patients remained asymptomatic until CSF pressure reached 68 mm Hg. Heilbrun, et al.,9 reported a remarkable decrease in CBF when ICP (EDP) reached 65 to 90 mm Hg and CPP decreased to 15 mm Hg. Lundberg, et al., 27 and P~lvSlgyW observed a reduction in rCBF in brain-tumor patients with increased ICP. The effect of increased ICP on CBF has been extensively investigated in animal experiments. The critical level of ICP that causes a reduction of CBF varies from 35 to 100 mm Hg, depending on the method of raising ICP. s,14,16,2~ As ICP affects CBF secondarily to changes in CPP, the effect of increased ICP on CBF should be investigated from the standpoint of CPP. 8,3~ The C P P is generally defined as the difference between MABP and ICP. s,ls,8~ The mechanism that maintains CBF during intracranial hypertension is equivalent to the process of CBF autoregulation that occurs during alterations in arterial pressure? The lower limit of CPP in CBF autoregulation is reported to be from 30 to 80 mm Hg in experimental animals. ~,saSag,3~ When a decrease in C P P is associated with an increase in ICP, maintenance of CBF becomes dependent on dilatation of the resistance vessels, that is, the decrease in CVR. Experimental reports have indicated a progressive fall in CVR and cerebrovascular dilatation in response to an increase in ICP. 14,15,~ Reports of cortical vasodilatation observed through a cranial window 4~ and vasodilatation seen on angiograms 27 support the concept of CVR decrease during intracranial 486
hypertension. The present results also showed that CVR decreased in every case during the plateau waves. The increased ICP created experimentally and the one observed during the plateau waves might be substantially different. The former is passive and the latter active and spontaneous; however, in either case, the CVR decreased. On the other hand, Kety, et al., TM concluded that CVR increased when ICP increased. This contradictory result might be explained by their calculations of CVR as MABP divided by CBF and the fact that ICP was not taken into account. Human studies showed a decrease in CBF ~7 and an increase in CBV 35 during the plateau waves. This discrepancy between CBF and CBV was explained by a shift of main CVR from the arterial to the venous side. ~8 In their experiments, Langfitt, et al., 22 and Grubb, et al.,7 reported an increase in CBV during increased ICP, while Lowell and Bloor ~5 reported a decrease. This decrease in CBV was attributed to loss of cerebral autoregulation. 7 The present study shows definitely that the plateau waves are accompanied or caused by a marked cerebral vasodilatation, and gives support to the report of CBV increase during the plateau waves, s5 However, what causes a marked cerebral vasodilatation is not yet known. Although it is one of the most potent cerebral vasodilators, CO~ is not likely to cause the plateau waves that appear and disappear abruptly in a matter of seconds, and, in this study, in the initial phase of the plateau waves PaCO~ was not increased at all. An increase in MABP observed during the plateau waves with CBF measurement in Cases 4 and 5 actually had occurred 15 to 20 minutes before the onset of the plateau waves. This MABP increase did not always accompany every plateau wave even in the same case, and this finding confirms the observation that the plateau waves occurred irrespective of variations of systemic blood pressure? e It is reported that the plateau waves are closely related to the intrinsic vasomotor control of J. Neurosurg. / Volume 50 / April, 1979
Plateau waves and cerebral hemodynamic changes cerebral circulation? 6a7,35 The m e c h a n i s m that can bring about a remarkable cerebral vasodilatation in a matter of seconds could be neurogenic. The plateau waves are observed in patients who are in an advanced stage of persistent intracranial hypertension with marked impairment of intracranial spatial compensation) 6a7 Many of the patients with brain tumor have disturbed autoregulation? T M The vasodilating ability was preserved in the patient in Case 5, who was in critical condition, with a very high ICP, and very low C P P and CBF. In conclusion, the plateau waves are caused by a marked cerebral vasodilatation and could occur as long as cerebral vasodilating ability is maintained, irrespective of the existence of cerebral autoregulation.
11.
12.
13.
14.
Acknowledgments
The authors are grateful to Mr. Tohru Fujita and Mr. Takao Mukai for their assistance in CBF measurements.
15.
References
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Address reprint requests to: Masayuki Matsuda, M.D., Department of Neurosurgery, Kyoto University Medical School, 54 Kawahara Cho, Shogoin, Sakyo Ku, Kyoto 606, Japan.
J. Neurosurg. / Volume 50 / April, 1979
