Journal of Neurology, Neurosurgery, and Psychiatry 1991;54:490-493

Single photon emission computed tomography inpatients with acute hydrocephalus or with cerebralischaemia after subarachnoid haemorrhage

Djo Hasan, Jacob van Peski, Ina Loeve, Eric P Krenning, Marinus Vermeulen

AbstractUsing single photon emission computedtomography (SPECT), cerebral bloodflow was studied in eight patients withgradual deterioration in the level ofconsciousness after subarachnoidhaemorrhage. Four had cerebralischaemia and four had acute hydro-cephalus. In patients with cerebralischaemia, single photon emission com-puted tomography scanning showedmultiple regions with decreased uptakeof technetium-99M labelled d,l-hexa-methyl-propylene amine oxime ("mTcHM-PAO) mainly in watershed areas. Inpatients with acute hydrocephalus,decreased uptake was seen mainly in thebasal parts of the brain: around the thirdventricle, around the temporal horns ofthe lateral ventricles, and in the basalpart of the frontal lobe. After serial lum-bar puncture, there was improvement ofthe uptake of 99mTc HM-PAO in thesebasal areas in three (convincingly in twoand slightly in the other) of the fourpatients accompanied by clinicalimprovement in these three patients.These results suggest that patients withacute hydrocephalus and impairedconsciousness after SAH, in contrast topatients with cerebral ischaemia, havedecreased cerebral blood flow predomin-antly in the basal parts of the brain.

University HospitalDijkzigt, Rotterdam,The NetherlandsDepartment ofNeurologyD HasanM VermeulenDepartment ofNuclear MedicineJ van PeskiI LoeveE P KrenningCorrespondence to:Dr Hasan, Department ofNeurology, UniversityHospital Dijkzigt Rotterdam,40 Dr Molewaterplein, 3015GD Rotterdam, TheNetherlandsReceived 29 June 1989and in final revised form27 April 1990.Accepted 18 May 1990

Many patients with cerebral ischaemia aftersubarachnoid haemorrhage have an impairedlevel of consciousness.' CT scanning andnecropsy studies in these patients demon-strated that brain damage was rarely restrictedto single vascular territories, but was usually a

multivascular and diffuse process.' These find-ings were confirmed by cerebral blood flow(CBF) study by means of positron emissiontomography (PET) in patients with cerebralischaemia after subarachnoid haemorrhage.2These multiple and bilateral lesions explainthe impairment of consciousness in thesepatients. Acute hydrocephalus may also beaccompanied by impaired consciousness,3 4perhaps mediated by a more global kind ofischaemia, since a reduction of cerebral bloodflow by enlarged ventricles has been demon-strated and in studies with '33Xenon.5'0

Recently, a new method to investigatechanges in the regional cerebral blood flow wasintroduced, by means of intravenously

administered technetium-99M labelled d,l-hexamethyl-propylene amine oxime (99mTcHM-PAO) and by the measurement of itsregional cerebral uptake by single photonemission computed tomography (SPECT)."The aim of this study was to compare the

pattern of cerebral blood flow, as depicted bySPECT scanning and 99mTc HM-PAO, inpatients with acute hydrocephalus with thosewith cerebral ischaemia after subarachnoidhaemorrhage.

Patients and methodsWe studied eight patients with subarachnoidhaemorrhage, four of them with delayedcerebral ischaemia, and four with acutehydrocephalus. All patients had suffered adeterioration of consciousness after admis-sion, defined as a sum score of 12 or less on the14 point Glasgow Coma Scale.'213 Aneurys-mal subarachnoid haemorrhage was confirmedby CT scanning on admission (initial CT).'4SPECT studies were performed whencerebral ischaemia or hydrocephalus was sus-pected to be the cause of the deterioration.Cerebral ischaemia was defined as a deteriora-tion of consciousness with or without focalneurological signs, and without hydro-cephalus or an enlarging haematoma on CT.Continuing deterioration immediately afteradmission was not regarded as cerebralischaemia. Acute hydrocephalus was diag-nosed if the bicaudate index, which wasmeasured on the initial CT or on a repeat CTwithin one week after the initial SAH,exceeded the normal upper limit (95t' percen-tile) for age,3 4 15 16 and if deterioration of cons-ciousness occurred with no detectable causeother than hydrocephalus.Technetium labelled HM-PAO is prepared

by adding 1110 megabecquerel freshly elutedsodium pertechnetate to a vial containingfreeze dried 0 5 mg d,l-hexamethyl-propyleneamine oxime (HM-PAO), 7 6 microgramstannous chloride dihydrate, and 4 5 mgsodium chloride (Ceretec). From this mixture,740 megabecquerel was intravenously admin-istered within 30 minutes after preparation.SPECT scanning was performed 10 to 20minutes later to avoid possible interferencefrom cerebral uptake of free sodium pertech-netate. Data acquisition was done by meansof a single-head rotating gamma-camera(Siemens) with a low energy all purposecollimator and a PDP 11/73 computer. Soft-ware: SPETS-1 1 running under TSX +,Nuclear Diagnostics. Total acquisition angle:

490

on 30 May 2019 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.54.6.490 on 1 June 1991. D

ownloaded from

Single photon emission computed tomography in patients with acute hydrocephalus or with cerebral ischaemia after subarachnoid haemorrhage 491

~~~~~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ _

Figure 1 Results of single photon emission computed tomography in patients with

cerebral ischaemia and in those with acute hydrocephalus after subarachnoid

haemorrhage. Horizontal lines on the transversal slices indicate the correspondingcoronal slices.

Key to fig 1

Without complicationsSPECT scan of cerebral uptake of 'Tc HM-PAO in a patient with subarachnoid

haemorrhage, who has no complication.

Cerebral ischaemia

Areas with decreased cerebral uptake of "mTc HM-PAO in patients with cerebral

ischaemia after subarachnoid haemorrhage (coronal and transversal slices):Case 1: left middle cerebral artery and left anterior and left posterior watershed

areas.

Case 2: in the territory of the right middle cerebral artery, right anterior and both

posterior watershed areas.

Case 3: right middle cerebral artery and both posterior watershed areas.

Case 4: left and right middle cerebral artery and anterior cerebral artery, rightanterior watershed area.

Acute hydrocephalus, before serial lumbar puncture

Areas with decreased cerebral uptake of "'Tc HM-PAO in patients with acute

hydrocephalus after subarachnoid haemorrhage, before serial lumbar puncture

Case 5, 6, 7 and 8:

transversal slices: around the ventricles, especially around the posterior horn of the

lateral ventricles. Case 5: diffusely distributed areas with decreased uptake of 'Tc

HM-PAO

coronal slices: around the third ventricle and the temporal horn of the lateral

ventricles in the basal parts of the brain. Case 7: a small area on the left side of the

lateral ventricle.

Acute hydrocephalus, after serial lumbar puncture

Areas with decreased cerebral uptake of ''Tc HM-PAO in patients with acute

hydrocephalus after subarachnoid haemorrhage, after serial lumbar puncture

Case 5, 6 and 7 (coronal slices):

changed pattern of 'Tc HM-PAO uptake in the basal parts of the brain (slightlyin Case 5, convincingly in Case 6 and 7).Case 8 (transversal and coronal slices):new multifocal areas with decreased cerebral uptake of ~'Tc HM-PAO, in the

territory of the right middle cerebral artery, in the right and left posterior-, and in

tright aerior-watrerheareas.

3600; 60 projections of 30 seconds each;64 x 64 matrix; pixel size: 6 mm. Spatialresolution for tomographic imaging(12 42 mm) was estimated by the calculationof the full width half maximum for 99mTcusing an air distance between the object andthe rotating collimator of 15 cm. Acquiredimages were filtered by means ofa Wiener filter(EMTFLT version 4- 1, by Sten Carlsson,Department of Medical Physics, S451-80Udevalla, Sweden). Transversal (parallel toorbito-meatal line), and coronal slices werereconstructed with a ramp filter, after correc-tion for attenuation, by calculation of thegeometric means. Slice thickness: 12 mm.The upper threshold was kept at 100% andthe lower at 5%. The reconstructed imageswere studied in the multi-slice, absolute scal-ing mode.

ResultsPatientsCerebral ischaemia was diagnosed in fourpatients (cases 1-4). Deterioration fromischaemia occurred between day 3 and day 9after subarachnoid haemorrhage. All had focalneurological signs: one patient had a righthemiparesis and aphasia (case 1); case 2 hadparesis of the left arm; case 3 had a lefthemiparesis; and the fourth patient (case 4) hada paralysis of the left leg and a righthemiparesis. None of the four patients had animpaired level of consciousness beforedeterioration from cerebral ischaemia. A repeatCT failed to show cerebral infarction in two(cases 1 and 3) of these four patients. A repeatCT in case 2 showed a hypodense area in theterritory of the right middle cerebral artery andin case 4 repeat CT showed a hypodense area inthe territory of the left anterior cerebral artery.Both hypodensities correlates with one of theareas with decreased cerebral uptake of 99mTcHM-PAO (fig 1) and with the focal neurologicaldeficits of these two patients.Another four patients deteriorated from

hydrocephalus (cases 5-8). The relativebicaudate indexes in these patients were: 1-30,1-30, 1 05, and 1*41. Deterioration from acutehydrocephalus occurred between day 1 and day4 after subarachnoid haemorrhage. After seriallumbar puncture, three of the four patientsshowed improvement of the level of conscious-ness. The remaining patient (case 8) developedcerebral ischaemia a few days after the onset ofdeterioration from acute hydrocephalus.

Spect StudiesIn patients with cerebral ischaemia, multiplecircumscribed areas with decreased uptake of99"TcHM-PAO were seen on the SPECT scan.The posterior watershed areas were involved inall patients and the anterior watershed areas inthree (cases 1, 2, and 4). Three patients (cases 2,3, and 4) had bilateral areas with decreaseduptake of 99"Tc HM-PAO (fig 1). The averagecounts/cell/minute of the patient without com-plications and of case 1, 2, 3 and 4 in the slicespresented in fig 1 were not different (1002/cell/min, 1074/cell/min, 1174/cell/min, 970/cell/min, and 906/cell/min respectively).

on 30 May 2019 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.54.6.490 on 1 June 1991. D

ownloaded from

Hasan, van Peski, Loeve, Krenning, Vermeulen

Table Relative average counts in patients with acutehydrocephalus. Regions of interest (A and B) are definedin fig 2

Relative average counts (region A/region B)

before LP* after LP*

Case 5 0 75 0 82Case 6 0-78 0-98Case 7 0-87 1 01Case 8 0 79 0 80

*LP = lumbar puncture.

In the four patients with acute hydro-cephalus, decreased uptake of 99mTc HM-PAOwas seen predominantly around the third ven-tricle, bilaterally in the basal parts of thetemporal lobes, around the temporal horns ofthe lateral ventricles, and in the basal parts ofthe frontal lobes. This pattern of areas withdecreased uptake is especially visible on thecoronal slices (fig 1) and the areas withdecreased uptake of S9mTc HM-PAO were byfar larger than the size of the third ventricle onCT (12 mm, 10 mm, 8 mm, and 1 1 mm respec-tively). In these patients there were only slightflow voids at the convexity of the brain. Seriallumbar puncture, which initially revealed highcerebro-spinal fluid pressures (40-50 cm H20),was performed in all four patients. RepeatedSPECT scanning after serial lumbar punctureshowed an improvement of the uptake of 9"mTcHM-PAO in the basal parts of the brain in case6 and 7, and a slight improvement in case 5.These changes were especially visible on thecoronal slices and were confirmed by compari-son of relative counts within the regions ofinterest (table and fig 2). Repeated SPECTscanning of the remaining patient (case 8), whodeveloped symptoms of cerebral ischaemia,showed decreased uptake of 9"mTc HM-PAO inboth posterior watershed areas, predominantlyon the left side, in the territory of the rightmiddle cerebral artery, and in the right anteriorwatershed area.

DiscussionSeveral studies have shown that cerebraluptake of ssmTc HM-PAO reflects cerebralblood flow."I 17 Decreased cerebral uptake of99mTc HM-PAO in cerebro-vascular diseasehas been shown to correspond well with theresults of other methods such as PET scan-

Figure 2 Regions ofinterest in patients withacute hydrocephalus. Theaverage relative countswere defined as averagecounts per cell per minuteof region A divided by thatof region B.

ning,18 19 and '33Xenon cerebral blood flowmeasurements .20

In our patients with impaired consciousnessfrom cerebral ischaemia, SPECT scanningshowed multiple regions with decreased uptakeof '9mTc HM-PAO, mainly in the watershedareas, reflecting impairment of cerebral bloodflow between the territories of the cerebralarteries. These areas with decreased uptake of99mTc HM-PAO agree with the distribution ofcerebral infarction described in necropsystudies in patients with subarachnoid haemor-rhage who had clinical symptoms of cerebralischaemia before death,' with one otherSPECT study using 99mTc HM-PAO,2' andwith CBF studies with PET2 in patients withcerebral ischaemia after subarachnoidhaemorrhage.

Multiple and bilateral distribution of areaswith decreased cerebral blood flow and sub-sequent brain ischaemia explains deteriorationin the level of consciousness in cerebralischaemia after subarachnoid haemorrhage butwhat is the cause of impaired consciousness inacute hydrocephalus? Decreased cerebralblood flow has been demonstrated in patientswith high9 and normal-pressure hydro-cephalus,5-8 '0 and may also be present in acutehydrocephalus, which would explain impair-ment of the level of consciousness. SPECTscanning indeed showed regions withdecreased uptake of 99mTc HM-PAO in ourhydrocephalic patients, but the pattern wasdifferent from that in patients with cerebralischaemia. In patients with acute hydro-cephalus, a decreased uptake was seenpredominantly in the basal parts of the brain.The areas with decreased uptake of `9mTc HM-PAO in the basal parts of the brain improvedconvincingly in two patients (case 6 and 7) andslightly in another patient (case 5), when com-pared with the higher parts of the brain, aftertreatment with serial lumbar puncture. Thiswas accompanied by clinical improvement inthese three patients. The patient who did notimprove had developed cerebral ischaemia.Decreased radio-activity in the basal areas in

patients with acute hydrocephalus cannot beexplained by compression of brain tissue by theenlarged ventricles without reduction of theregional blood flow, because in that case eachunit of volume of the compressed brain tissuewould have shown a higher radio-activity onthe SPECT scan. Moreover, brain tissue doesnot compress but shifts outward and upwarddisplacing CSF. The decreased uptake cannotbe explained by a partial volume phenomenonfrom the third ventricle because the area ofdecreased uptake is far larger than that of thethird ventricle on CT. The decreased uptakemost likely reflects decreased cerebral bloodflow, but the question is whether there is aprimarily decreased cerebral blood flow or adecreased blood flow secondary tohypometabolism. A primary disturbance ofcerebral blood flow is the most likely explana-tion since it was shown in patients with recent-onset obstructive hydrocephalus associatedwith cerebral neoplasia that the levels ofcortical blood flow were inappropriately low

492

on 30 May 2019 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.54.6.490 on 1 June 1991. D

ownloaded from

Single photon emission computed tomography in patients with acute hydrocephalus or with cerebral ischaemia after subarachnoid haemorrhage 493

compared with the levels of cortical oxygenutilisation.22 The pattern of regional cerebralblood flow impairment that we found in patientswith hydrocephalus has not been reportedbefore. In most studies,5689 however, non

rotating, multiple collimated scintillationdetectors were used, and cerebral blood flowvalues of the grey matter were estimated bycalculating the initial slope index of the"'Xenon clearance curve21 24 orby analysing thegrey matter part of the bicompartmentalmodel.2324 Obviously changes in the blood flowto the deep regions of the brain cannot bedetected with this method. Others measuredregional cerebral blood flow by means ofSPECT and "'Xenon,710 but calculatedregional cerebral blood flow from slices of atleast 5 cm above the orbito-meatal line. Theseslices are well above the areas of decreasedregional cerebral blood flow found in our

patients.Apart from showing that impaired

consciousness in acute hydrocephalus resultsfrom a disturbance predominantly in the basalparts of the brain, this study may also havepractical implications. If a patient hasdeteriorated from acute hydrocephalus anddoes not respond to treatment, the explanationmay be that insufficient cerebro-spinal fluiddrainage or another complication such as

cerebral ischaemia has developed. The latter ismost likely if SPECT scanning showsdecreased regional cerebral blood flow else-where than in the basal parts of the brain, even

if CT shows no evidence of infarction.

We are grateful to Professor Jan van Gijn for his comments, toMrs Betty Mast for her excellent secretarial help, and toAmbroos Reijs for technical assistance.

1 Hijdra A, van Giin J, Stefanko S, van Dongen KJ,Vermeulen M, van Crevel H. Delayed cerebral ischemiaafter aneurysmal subarachnoid hemorrhage. Clinico-anatomic correlations. Neurology 1986;36:329-33.

2 Powers WJ, Grubb RL, Baker RP, Mintun MA, RaichleME. Regional cerebral blood flow and metabolism inreversible ischemia due to vasospasm. Determination bypositron emission tomography. J Neurosurg 1985;62:539-46.

3 Van Gijn J, Hijdra A, Wijdicks EFM, Vermeulen M, van

Crevel H. Acute hydrocephalus after aneurysmal sub-arachnoid hemorrhage. J Neurosurg 1985;63:355-62.

4 Hasan D, Vermeulen M, Wijdicks EFM, Hijdra A, van Gijn

J. Management problems in acute hydrocephalus aftersubarachnoid hemorrhage. Stroke 1989;20:747-53.

5 Mamo HL, Philippe CM, Ponsin JC, Rey AC, Luft AG,Seylaz JA. Cerebral blood flow in normal pressurehydrocephalus. Stroke 1987;18:1074-80.

6 Menon BW, Weir B, Overton T. Ventricular size andcerebral blood flow following subarachnoid hemorrhage.J Comput Assist Tomogr 1981;5:328-33.

7 Vorstrup S, Christensen J, Gjerris F, Sorensen S, ThomsenAM, Paulson OB. Cerebral blood flow in patients withnormal pressure hydrocephalus before and after shunting.J Neurosurg 1987;66:379-87.

8 Tamaki N, Kusunoki T, Wakabayashi T, Satoshi M.Cerebral hemodynamics in normal pressure hydro-cephalus. Evaluation by '3Xe inhalation method anddynamic computed tomography study. J Neurosurg1984;61:510-14.

9 Hayashi M, Kobayashi H, Kawano H, Yamamoto S, MaedaT. Cerebral blood flow and intracranial pressure patternsin patients with communicating hydrocephalus aftersubarachnoid hemorrhage. J Neurosurg 1984;61:30-6.

10 Graff-Radford NR, Rezai K, Goderski JC, Eslinger P,Damasio H, Kirchner P. Regional cerebral blood flow innormal pressure hydrocephalus. J Neurol NeurosurgPsychiatry 1987;50: 1589-96.

11 Neirinckx RD, Canning LR, Piper IM, et al. Technetium-99M d,l-HM-PAO: a new radiopharmaceutical forSPECT imaging of regional cerebral blood perfusion. JNuclMed 1987;28:191-202.

12 Teasdale GM, Jennett B. Assessment of coma and impairedconsciousness. A practical scale. Lancet 1974;ii:81-4.

13 Lindsay KW, Teasdale GM, Knill-Jones RP. Observervariability in assessing the clinical features of subarach-noid hemorrhage. J Neurosurg 1983;58:57-62.

14 Van Gijn J, Van Dongen KJ. Computed tomography insubarachnoid hemorrhage, difference between patientswith and without an aneurysm on angiography. Neurology1980;30:538-9.

15 Earnest MP, Heaton RK, Wilkinson WE, Manke WF.Cortical atrophy, ventricular enlargement and intellectualimpairment in the aged. Neurology 1979;29:1 138-43.

16 Meese W, Kluge W, Grumme T, Hopfenmuller W. Com-puted tomography evaluation of the cerebro-spinal fluidspaces of healthy persons. Neuroradiology 1980;19:131-6.

17 LearJL. Quantitative local cerebral blood flow measurementwith technetium-99M HM-PAO: evaluation using mul-tiple radionuclide digital quantitative autoradiography.J Nucl Med 1988;29:1387-92.

18 Nishizawa S, Yonekura Y, Fujita T, et al. Brain perfusionsingle photon emission computed tomography with "'TcHM-PAO: comparative study with I-123 IMP andcerebral blood flow measured by positron emissiontomography (Abstract). J NuclMed 1987;28:569.

19 Yonekura Y, Nishizawa S, Mukai T, et al. SPECT with"Tc-d,l-hexamethyl-propylene amine oxime (HM-PAO) compared with regional cerebral blood flowmeasured by PET. Effects of linearisation. J Cereb BloodFlow 1988;-:S82-S89.

20 Andersen AR, Friberg H, Lassen NA, Kristensen K,Neirinckx RD. Serial studies on cerebral blood flow using"'Tc HM-PAO: a comparison with "'Xe. Nucl MedComm 1987;8:549-57.

21 Davis S, Andrews J, Lichtenstein M, et al. A single-photonemission computed tomography study of hypoperfusionafter subarachnoid hemorrhage. Stroke 1990;21:252-9.

22 Brooks DJ, Beaney RP, Powell M, et al. Studies on cerebraloxygen metabolism, blood flow, and blood volume inpatients with hydrocephalus before and after de-compression, using positron emission tomography. Brain1986;109:613-28.

23 Lassen NA. Cerebral blood flow measured by xenon-133.Nucl Med Comm 1987;8:535-48.

24 Geraud G, Tremoulet M, Guell A, Bes A. The prognosticvalue of noninvasive cerebral blood flow measurement insubarachnoid hemorrhage. Stroke 1984;15:301-5. on 30 M

ay 2019 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.54.6.490 on 1 June 1991. Dow

nloaded from