To-cmd-Fro Movement and External Escape

of Carotid Arterial Blood in Brain Death

Cases. A Doppler Ultrasonic Study
BY SHOTARO YONEDA, M.D.,* AKIFUMI NISHIMOTO, M.D.,* TADAATSU NUKADA, M.D.,* YOSHIHIRO
KURIYAMA, M.D.,* KIKUSHI KATSURADA, M.D.,t AND HIROSHI ABE, M.D.*

Abstract: • In brain death cases who showed nonfilling phenomena in the internal carotid angiograms,
To-and-Fro the blood flow velocity patterns of the common carotid arteries were characterized by involve-
Movement
and External ment of a single systolic peak and a marked reverse flow component which had never been
Escape of observed in healthy subjects.
Carotid Arterial The individuality of each blood flow velocity pattern in the common, internal and external
Blood in carotid arteries was made clear by placing the transducer in contact with the respective artery in
Brain Death
Cases. A a certain case. The Doppler signal from the internal carotid artery involving a signal from a
Doppler reverse flow was slightly detectable, even if the blood pressure was elevated by norepinephrine
Ultrasonic infusion and the external carotid artery was temporarily compressed. The blood flow velocity
Study pattern of the external carotid artery was similar to the pattern of the common carotid artery.
The peculiar flow pattern indicates that a brain death case has a to-and-fro movement in the in-
ternal carotid blood flow and an external carotid escape of common carotid arterial blood.

Additional Key Words Doppler signal blood flow velocity pattern

transcutaneous Doppler flowmeter nonfilling phenomenon reverse flow

Introduction primary diseases were cerebral contusion (three), sub-

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• Individuals with brain death have effectively lost
cerebral circulation. This evidence has been shown
with angiography,1"4 the radioisotope method 512 and
the N 2 O method.13
Since Satomura (I960)14 developed an ultrasonic
flowmeter based upon the Doppler effect, and
Franklin (1961)16 used it in blood flow measurement of
animals, further progress in the instrumentation led to
the development of a transcutaneous Doppler
flowmeter by which blood flow velocity was able to be
detected through the skin. Ultrasonic Doppler
technique as a noninvasive method has been used for
detecting carotid blood flow1620 and has been applied
to extracranial vascular diseases.21'22 It may be possi-
ble to assume cerebral hemodynamics by measure-
ment of carotid blood flow velocity.
The purpose of the present investigation was to
study blood flow velocity patterns of carotid arteries in
patients with brain death whose cerebral circulation
was extremely disturbed.
Methods
The series consisted of ten patients with brain death. The
From the *Department of Internal Medicine and the tlntensive
Care Unit, Osaka University Hospital, Fukushima, Osaka-553,
Japan.
Supported in part by Takeda Medical Research Foundation,
No. 47-3, Osaka, Japan.
arachnoid hemorrhage (three), subdural hematoma (two),
epidural hematoma (one) and intraperitoneal hemorrhage
(one). The criteria of brain death were followed according to
the Ad Hoc Committee of the Harvard Medical School.23
Carotid angiography, electroencephalography and Doppler
flowmetry were performed in all cases.
The carotid blood flow velocity pattern was detected by
a directional Doppler rheogram (HITACHI EUD-2A, 5 M
Hz). The method was originally described by Kato and
Izumi.24
Results
The medical records of ten cases are summarized in
table 1. Age, sex, diagnosis, findings of carotid
angiogram (CAG) and electroencephalogram (EEG),
pressure of cerebrospinal fluid (CSF) and systemic
arterial blood pressure were presented in this table. In
all cases, the carotid angiograms revealed nonfilling
phenomena (figs. 1 and 2).
Figures 3 through 6 show the blood flow velocity
patterns of the common carotid arteries in cases 4, 6, 8
and 9. The blood flow velocity patterns in these four
cases were characterized by a single systolic peak and
a reverse flow component. The patterns in the other
six cases also showed the same pattern as shown in
these figures (table 2).
It is possible that the transducer was placed in
contact with the common, internal and external
carotid arteries of case 9. As shown in figure 6, the
blood flow velocity pattern of the common carotid

Stroke, Vol. 5, November-December 1974 707

 YONEDA, NISHIMOTO, NUKADA, KURIYAMA, KATSURADA, ABE

TABLE 1

Cates of Brain Death

CSP prossur* Blood pr«ssar«
C u t no. Ag. Diagnosis CAO no (mm Hg) (mm Hg)

1 51 M Subdural hematoma Nonfllling Flat 96/68

2 43 M Cerebral contusion Nonfilling Flat 100 116/70
3 40 M Subdural hematoma Nonfllling Flat 80 96/68
4 40 M Subarachnoid hemorrhage Nonfllling Flat — 110/70
5 21 M Epidural hematoma Nonfllling Flat — 80/30
6 25 F Subarachnoid hemorrhage Nonfllling Flat —. 110/90
7 23 M Cerebral contusion Nonfllling Flat — 120/60
8 17 M Cerebral contusion Nonfllling Flat — 130/80
9 29 M Subarachnoid hemorrhage Nonfllling Flat — 94/70
10 4 F Intraperitoneal hemorrhage Nonfllling Flat — 120/90
CSF: cerebrospinal fluid.
CAG: carotid angiography.
EEG: electroencephalography.

artery in this case was similar to the transcutaneous systolic peaks (Si and Sj) and a following diastolic
Doppler pattern which consisted of a single systolic peak (D) and that a slight reverseflowbetween systole
peak and a reverse flow. The Doppler signal from the and diastole is sometimes observed26 (fig. 9). The
internal carotid artery producing the signal from reverse flow in patients with brain death was promi-
reverse flow was barely detectable. The blood flow nent in comparison with a slight reverse flow in
velocity pattern of the external carotid artery was healthy subjects. Matsuo and Nimura" described
similar to the pattern of the common carotid artery. patients with aortic valvular insufficiency (AI) and
With temporal compression of the external carotid
artery, the Doppler signal from the common carotid
artery became scarcely detectable (fig. 7). An increase
in systolic arterial blood pressure by norepinephrine
infusion (from 94/70 to 220/174 mm Hg) produced
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little change in blood flow velocity pattern of the inter-

nal carotid artery. The blood flow velocity pattern of
the common carotid artery was similar to the pattern
of the external carotid artery (fig. 8).

Discussion
It is known that the blood flow velocity pattern of the
common carotid artery in healthy subjects shows two

P1GURI 1 FIGURI2

Carotid angiogram of case I. Nonfilling phenomena of the internal Carotid angiogram of case S. Internal carotid angiogram did not
carotid angiogram and external carotid angiogram were observed. appear, while external carotid angiogram was observed.

Strot., Vol. 5, Nonmbtr-DKtmbv 1974

 OOPPLIR ULTRASONIC STUDY

A.carotis comm.

ECG

5KHz

i.

base line
Reverse flow

ECG

Isec
F10UU 1
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The blood flow velocity pattern of case 5. Moderate reverse flow and a single systolic peak were observed in the common
carotid artery.

with idiopathic hypertrophic subaortic stenosis mal subjects appeared in the common and external
(IHSS) who had a reverse flow component in their carotid arteries of brain death cases.
common carotid artery. The cases in this study did not In one case (case 9) whose bloodflowvelocity was
have AI and IHSS. A single systolic peak of the blood measured by placing the transducer in contact with the
flow velocity pattern which was not observed in nor- carotid arteries, the blood flow velocity pattern of the
common carotid artery producing the reverseflowwas
similar to the pattern of the external carotid artery.
The Doppler signal from the internal carotid artery
TABLE 2
producing the signal from reverseflowcould be barely
Blood Flow Velocity Patterns of Common Carotid Arteries detected, even if arterial blood pressure was elevated.
of Cases With Brain Death With temporal compression of the external carotid
Cai» no. Ravar»e flow Singla •y«tollc pmak artery, the Doppler signal from the common carotid
artery became scarcely detectable. These findings in-
1 + + dicated that almost all of the blood of the common
2 + + carotid artery flowed into the external carotid artery.
3 ++ + In other words, there was an external carotid escape of
4 ++ + common carotid arterial blood. It is accepted in brain
5 ++ +
6 +++ + death that the cerebral angiogram shows nonfilling
7 ++ + phenomena1"4 and that cerebral blood flow is ex-
8 +++ + tremely reduced.*"' It also is known that the in-
9 + + tracranial pressure of patients with brain death
10 + + increases to the same level as arterial blood pres-
sure.'1 "• " Therefore, the cerebral perfusion pressure
+ : Mild reverse flow, +-)-: moderate reverse flow, + + + :
marked reverse flow.
is equal to or near zero. The previous reports about

Slrok; Vol. 5, NoKH,.b«r-DKtmb«r 1974 709

 YONIDA, NISHIMOTO, NUKADA, KURIYAMA, KATSURADA, ABI

A. carotis comm.

4 KHz

base line
1
2
ECG
* KHz
3

i 2
1

'
w If
rtevws* f l o w '
base U n a
1
2
ECG
FIOUM 3
flow *»"
The blood flow velocity pattern of case 8. The blood flow velocity
pattern of the common carotid artery showed marked reverse flow
ECG and a single systolic peak.

FIOUM 4

The blood flow velocity pattern of case 6. Marked reverse flow

was presented in the blood flow velocity pattern of the common
carotid artery.
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DOPPLER SONOGRAMS OF THE CAROTID ARTERIES OF BRAIN DEATH

A.M., 2 9, male Brain death after head injury with contused wound of the neck
4 KHz
!
2
Impossible to detect

' • - V ^ base line

the internal carotid f l o w Reverse flow
Reverse flow

A. by the percutaneous method

A
Comm. Carotid A.(percutaneous) int. Carotid A. (percutaneous) Ext. Carotid A. (percutaneous)

4 KHz
3
?
> •

Reverse flow
A *
Reverse flow
JL 1
l»bas* line
1
Reverse flow

Comm. Carotid A. (direct) Int. Carotid A. (direct) Ext. Carotid A. (direct)

The blood flow velocity pattern of case 9. "Direct" showed the blood flow velocity pattern that a transducer was placed in contact with the
common, internal and external carotid arteries respectively. Doppler signal from the internal carotid artery was slightly detectable.

7X0 Slrolct, Vol. 5, Noytmbtr-Dtctmbtr 1974

 DOPPLIR ULTRASONIC STUDY

R. A. carotis comm.

Reverse flow

• r" »

R. A. carotis comm.
R. A. carotis int.

Reverse flow

Reverse flow

ECG
A /I
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E C G

-
R. A. carotis int. R. A. carotis ext.

' , . ^
Reverse flow

Reverse flow

ECG
ECG

FIGURE S

The blood flow velocity pattern of case 9 at compression of the The blood flow velocity pattern of case 9 at elevation of arterial
external carotid artery. Doppler signal from the common carotid blood pressure (from 94/70 to 220/174 mm Hg). The blood flow
artery was scarcely detected. velocity pattern of the internal carotid artery was barely observed.

Slrokt, Vol. 5, Novunbw-Dtctmbtr 1974 711

 YONEDA, NISHIMOTO, NUKADA, KURIYAMA, KATSURADA, ABI
Si
The blood flow velocity pattern of the common carotid artery in a
normal subject. Note two systolic peaks (S, and S,), a diaslolic peak
(D) and a little reverse flow.
brain death support the existence of external carotid
escape of common carotid arterial blood.
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It had been reported that percutaneous injection
of 133Xe, even if it was performed selectively into the
internal carotid artery with the catheter tip near to the
siphon, was always followed by extracranial tracer
contamination and clearance."110 It was considered,
therefore, that the blood flow velocity pattern of the
internal carotid artery indicated a to-and-fro move-
ment of internal carotid arterial blood synchronizing
with each heart beat. The blood flow velocity pattern
of the common carotid artery may originate from a
to-and-fro movement of the blood in the internal
carotid artery and some factors in the periphery of the
external carotid artery.
References
1. Riishede J, Ethelberg S: Angiographic changes in sudden and
severe herniation of brain stem through tentorial incisure.
Arch Neurol Psychiat 70:399-409 (Sept) 1953
2. tangfift TW, Kassell NF: Non-filling of cerebral vessels dur-
ing angiography. Acta Neurochir 14:96-104, 1966
3. Mitchell OC, De ta Torre E, Alexander E, et ah The non-filling
phenomenon during angiography in acute intracranial
hypertension. J Neurosurg 19:766-774 (Sept) 1962
4. Bergquist E, Bergstrom K: Angiography in cerebral death.
Acta Radiol 12:283-288 (May) 1972
5. Baldy-Moulinier M, Frerebeau Ph: Blood flow of the cerebral
cortex in intracranial hypertension. Scand J Clin tab Invest
2 2 (Suppl 102):V:G, 1968
6. Hadjidimos AA, Brock M, Baum P, et ah Cessation of
712
cerebral blood flow in total irreversible loss of brain func-
tion. In Brock M, Fieschi C, Ingvar DH, et al (eds): Cerebral
Blood Flow. Berlin, Springer-Verlag, pp 209-212, 1969
7. Baldy-Moulinier M, Frerebeau Ph: Cerebral blood flow in
cases of coma following severe head injury. In Brock M,
Fieschi C, Ingvar DH, et al (eds): Cerebral Blood Flow. Berlin,
Springer-Verlag, pp 216-218, 1969
8. Brock M, Schurmann K, Hadjidimos AA: Cerebral blood flow
and cerebral death. Acta Neurochir 2 0 l 195-209, 1969
9. J^rgensen PB, Heilbrum MP, Boysen G, et ah Cerebral perfu-
sion pressure correlated with regional cerebral blood flow,
EEG and aortocervical arteriography in patients with severe
brain disorders progressing to brain death. Europ Neurol
8:207-212, 1972
10. Bes A, Arbus L, tazorthes Y, et ah Hemodynamic and
metabolic studies in "Coma Depasse." A search for a
biological test of death of the brain. In Brock M, Fieschi C,
Ingvar DH, et al (eds): Cerebral Blood Flow. Berlin, Springer-
Verlag, pp 213-215, 1969
11. Goodman JM, Mishkin FS, Dyken M: Determination of brain
death by isotope angiography. JAMA 209:1869-1872
(Sept) 1969
12. Braunstein P, Korein J, Kricheff I, et al: A simple bedside
evaluation for cerebral blood flow in the study of cerebral
death: A prospective study of 34 deeply comatose patients.
Amer J Roentgen 1 18:757-767 (Aug) 1973
13. Shalit MN, Beller AJ, Feinsod M, et ah The blood flow and
oxygen consumption of the dying brain. Neurology 20:740-
748 (Aug) 1970
14. Satomura S, Kaneko Z: Ultrasonic blood rheograph.
Proceedings of the Third International Conference of Medical
Electronics, tondon, International Federation for Medical
Electronics, p 254-258, 1960
15. Franklin DL, Schlegel W, Rushmer RF: Blood flow measured
by Doppler frequency shift of back-scattered ultrasound.
Science 134:564-565 (Aug) 1961
16. Goldberg RE: Doppler physics and preliminary report of a
test for carotid insufficiency. In Goldberg RE, Sarin LK (eds):
Ultrasonics in Ophthalmology; Diagnostic and Therapeutic
Applications. Philadelphia, WB Sounders, pp 199-200, 1967
17. Grossman Bt, Wood EH: Evaluation of cerebrovascular dis-
ease utilizing a transcutaneous Doppler technique.
Radiology 90:586-587 (Mar) 1968
18. Kristensen JK: Carotid and vertebral blood flow evaluation
by means of ultrasound. Acta Neurol Scond 4 3 (Suppl
31):116, 1967
19. Miyazaki M, Kato K: Measurement of cerebral blood flow by
ultrasonic Doppler technique. Hemodynamic comparison of
right and left carotid artery in patients with hemiplegia. Jap
Circ J 29:383-386 (Apr) 1965
20. Benchimol A, Barreto EC, Goldstein MR, et ah Measurement
of phasic carotid artery flow velocity in man. Amer J Med
49:170-174 (Aug) 1970
21. Brinker RA, Landiss DJ, Croley TF: Detection of carotid artery
bifurcation stenosis by Doppler ultrasound. J Neurosurg
29:143-148 (Aug) 1968
22. Brisman R, Grossman Bt, Correll JW: Accuracy of
transcutaneous Doppler ultrasonics in evaluating ex-
tracranial vascular disease. J Neu-osurg 32:529-533 (May)
1970
23. Report of Ad Hoc Committee of the Harvard Medical School
to examine the definition of brain death: A definition of
irreversible coma. JAMA 205:337-340 (Aug) 1968
24. Kato K, Izumi Z: A new ultrasonic Doppler flowmeter that can
detect flow directions. Med Ultrason 3:28-29, 1967
Slrok; Vol. 5. Novmbv-Dtctmbv
 DOPPLER ULTRASONIC STUDY
25. Matsuo H, Nimura Y: Analysis of flow patterns in blood
vessels with a directional ultrasonic Doppler technique
through a transcutaneous approach. Jap Circ J 37:735-746
(July) 1973
26. J^rgensen PB, J^rgensen EO, Rosenklint A: Brain death.
Downloaded from http://ahajournals.org by on April 1, 2022
Stroke, Vol. 5, November-December 1974
Pathogenesis and diagnosis. Acta Neurol Scand 49:355-
367, 1973
27. Yamauchi Y, Katsurada K, Nukada T, et al: An application of
echoencephalography to non-perfused and luxury perfused
human brains. Med J Osaka Univ 24:101-109 (Sept) 1973
713