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Perspectives in Medicine (2012) 1, 362—365
Bartels E, Bartels S, Poppert H (Editors):
New Trends in Neurosonology and Cerebral Hemodynamics — an Update.
Perspectives in Medicine (2012) 1, 362—365
journal homepage: www.elsevier.com/locate/permed
The role of color duplex sonography in the brain
death diagnostics
Igor D. Stulina, Denis S. Solonskiya,∗, Mikhail V. Sinkinb, Rashid S. Musina,
Alexandr O. Mnushkina, Alexey V. Kascheeva, Leonid A. Savina,
Mikhail A. Bolotnovc
aMoscow State University for Medicine and Dentistry, Department of Neurology, Russia
bMoscow Clinical Hospital 11, Russia
cMoscow Clinical Hospital 13, Russia
KEYWORDS
Brain death;
Transcranial Doppler
sonography;
Cerebral blood
arrest;
Confirmatory test
Summary In Russia brain death diagnostic is still under great public attention. In such envi-
ronment confirmatory tests are absolutely necessary. Aim of our study is to investigate the
cerebral blood flow in brain death using color-coded duplex sonography. The sonographic study
of 20 patients with brain death was performed and included transcranial and extracranial color
duplex sonography. All patients were untrepanized. The following parameters were measured
— presence of reverberating flow, Vmax ranges.
Results: At baseline TCDS revealed both MCA in all patients, and the BA in 18 patients.
Oscillating flow with Vmax −32 ±12 sm/s in MCA was found. Reverberating flow in the proximal
segment of ICA and in the V2 segment of VA was found in all patients. Vmax ranges were
96 ±27 sm/s in ICA and 58 ±17sm/s in VA. After 6 h TCDS was successful in 16 patients. In all
of 16 cases blood flow in the MCA as a systolic peak or reverberating flow was detected. Basilar
system study was successful in 12 cases. In all vessels blood flow was as systolic peaks.
Extracranial ICA and VA were visualized in all cases. In the ICA and V2, V3 segments of
the VA reverberating flow were detected. Vmax was 47 ±25 sm/s in ICA and 35±17 sm/s in
VA. In BD color duplex scanning reveals oscillating flow or systolic spikes in distal ICA, VA,
intracranial vessels. In TCDS, the most common finding is MCA with reverberating flow. The
optimum combination is extracranial and intracranial scanning in the early stages of BD.
Introduction
The brain death (BD) is defined as the irreversible loss of
function of the brain, including the brainstem, develop-
ing on the assumption of pulmonary ventilation and heart
∗Corresponding author. Tel.: +7 9175878262.
E-mail address: dsolonsky@hotmail.com (D.S. Solonskiy).
beating. The BD is diagnosed in intensive care units (ICU) as
a result of severe brain damaging and causes at least 10%
of mortality in ICU in developed countries. Traumatic brain
injury, malignant stroke, tumor, diffuse hypoxic—ischemic
brain damage are supposed to be the main causes of BD. All
these factors affect the brain and lead to brain edema and
swelling, intracranial pressure increase, gradual reduction
of cerebral perfusion pressure, decrease and termination of
intracranial blood flow and necrosis of brain parenchyma up
to 2nd cervical segment [1—3].
2211-968X © 2012 Elsevier GmbH.
http://dx.doi.org/10.1016/j.permed.2012.03.002
Open access under CC BY-NC-ND license.
Open access under CC BY-NC-ND license.
The role of color duplex sonography in the brain death 363
According to the Russian National Guidelines of BD there
are Diagnostic criteria for clinical diagnosis of BD [4]:
1. Defined cause irreversible deep coma.
2. Exclusion of complicating medical conditions that may
confound clinical assessment (absence of hypothermia,
drug intoxication, severe electrolyte and endocrine dis-
turbance).
3. Systolic blood pressure ≥90 mm Hg.
4. Absence of brainstem reflexes.
5. Mydriasis with no response to the bright light.
6. Apnea with arterial pCO2≥60 mm Hg.
7. The observation period of 6 and 24 h with the primary
and secondary brain injury respectively.
In general, these criteria correspond to neurologic crite-
ria for the diagnosis of brain death of American Academy of
Neurology [2,5].
The following two confirmatory tests are approved for BD
diagnosis in Russia:
1. Electroencephalography (EEG) — reveals no electrical
activity of brain in BD patients.
2. Cerebral angiography — detects cerebral blood arrest in
BD patients.
Angiography is believed to reduce the observational
period only and does not substitute to any clinical criteria of
BD. According to the Russian National Guidelines on Diagnos-
tics of Brain Death, ultrasound confirmatory tests are being
investigated and can not be recommended for BD diagnosis,
at the same time, all over the world ultrasound tests are
the 3rd in order of sensitivity and frequency for BD diagnos-
tics [6,7]. Transcranial Doppler (TCD) is notably desirable in
patients in whom specific components of clinical testing can-
not be reliably performed or evaluated such as barbiturate
brain protection, hypothermia or face trauma [8—10].
Our department has gained experience in ultrasonogra-
phy in clinical and confirmatory tests, 438 cases of BD were
diagnosed since January 1995 to December 2010 [11]. The
diagnosis of BD was confirmed by TCD and EEG. Color duplex
sonography (CDS) was started to be performed in 2009.
We initiated a prospective observational study of the
extra- and intracranial artery CDS in BD diagnostics in 2009.
20 patients with BD have been enrolled in the study up to
December 2010. The study was approved by Local Ethic Com-
mittee of Moscow State University for Medicine and Dentistry
in 2008.
The aim of the study was
- to investigate whether CDS of both extra- and intracranial
arteries increases sensitivity of the test in patients with
BD compared with CDS of intracranial arteries alone;
- to clarify CDS criteria of circulatory blood arrest.
Materials and methods
The study was started in Moscow hospital intensive care units
in 2009 and has still been going on.
20 patients with BD due to traumatic brain injury and
intracranial hemorrhage were included in the study and
Table 1 Systolic velocity ranges in extra- and intracranial
arteries.
Systolic
velocity
ICA
(sm/s)
VA
(sm/s)
MCA
(sm/s)
BA
(sm/s)
1ast exam 96 ±27 58 ±17 32 ±12 38 ±9
2nd exam 47 ±25 35 ±17 15 ±821±7
underwent a sonographic study which included color duplex
sonography (CDS) of extracranial and intracranial arteries.
BD was diagnosed according to the Russian National
Guidelines of BD. The average age of patients was 25 ±5.4
years. The average time from ICU admission to BD devel-
opment was 27 ±6.5 h. The diagnosis of traumatic brain
injury and intracranial hemorrhage was detected by com-
puter tomography at the admission. All the patients had
severe diffuse brain injury with the transverse and axial
dislocation. Craniotomy was not carried on.
The sonographic study was performed according to the
Rules of Task Force Group on Cerebral Death of Neurosonol-
ogy Research Group of the World Federation of Neurology
[12].
The following criteria of the test were mandatory:
1. The investigation of anterior and posterior circulation.
2. Bilateral visualization of intracranial internal carotid
artery branches.
The study was conducted on a portable device Sonosite
Micromaxx (USA) with broadband transducers L5—10 mHz,
P1—5 mHz twice: at baseline after assessment of clinical cri-
teria of BD and 6 h later. Presence of reverberating flow,
Vmax ranges, presence of midline shift in B mode were also
measured.
Results
At baseline CDS revealed both MCA (right and left) in all
20 patients, both ACA in 16 patients and BA in 18 patients.
Oscillating flow with Vmax −32 ±12 sm/s in MCA was found.
Data of extra- and intracranial artery and blood flow rates
are presented below (Tables 1 and 2).
A midline shift 4—10 mm in B-mode was noted in 13
patients and it made artery differentiation difficult.
Reverberating flow in the proximal segment of ICA and in
the V2 segment of VA was found in all patients.
Vmax ranges were 96 ±27 sm/s in ICA and 58 ±17 sm/s
in VA respectively.
Reverberating and oscillating flow of intracranial and
extracranial artery are presented in Figs. 1—4.
Table 2 Visualization frequency of extra- and intracranial
arteries (n= 20).
N= 20 MCA ACA PCA BA VA V2 ICA prox
1st exam 20 16 15 18 20 20
2nd exam 16 11 5 12 20 20
364 I.D. Stulin et al.
Figure 1 Reverberating flow in MCA in case of brain death.
After 6 h TCCS was successful in 16 patients. In all of 16
cases blood flow in the MCA as a systolic peak or reverber-
ating flow was detected.
Extracranial ICA and VA were visualized in all cases. In the
ICA and V2, V3 segments of the VA reverberating flow were
detected. Vmax was 47 ±25 sm/s in ICA and 35 ±17 sm/s in
VA. Spontaneous echo contrast in ICA and bulb was observed
in 14 cases.
Thus, the sensitivity of the method in extra and intracra-
nial study was 100%. The separate holding TCD in early
sensitivity was 90%, at a later date from the time of clinical
brain death sensitivity decreased to 80%.
Discussion
Brain death is a clinical diagnosis and neurologic crite-
ria are still the main valid in BD diagnosis. However BD
diagnosis has a comprehensive ethic value and on the one
hand, there are some patients in whom specific compo-
nents of clinical testing cannot be reliably performed or
evaluated. Thus new maximal accurate, fast and safe test
for BD diagnosis are required. On the other hand, fre-
quently spontaneous and reflex movements, face trauma
make difficulties of the BD diagnostics that is why additional
Figure 2 Systolic spikes in MCA in case of brain
death.
Figure 3 Reverberating flow in ICA (extracranial) in case of
brain death.
confirmatory tests are considered to trend in unclear cases.
Moreover, significant restriction of observational period or
complete rejection of re-examination for BD diagnosis is
discussed when confirmatory tests are performed [2,8,13].
All the tests for BD diagnosis perfectly have to be:
(a) feasible at the bedside;
(b) survey should not take much time;
(c) should be safe for the examinee, and a potential recipi-
ent of donor organs as well as performing their medical
staff;
(d) to be sensitive, specific, reproducible and protected
from external factors.
Color duplex scanning is the test which satisfies better
than others to the requirements listed above. The great
advantage of duplex scanning compared with the blind
Doppler in BD is an opportunity of direct visualization of
the lumen, which facilitates the diagnostics.
The most important is the qualitative analysis of the
spectrograms with the definition of specific patterns of oscil-
lating or reverberating flow, indicating the development of
circulatory blood arrest. Quantitative parameters, including
Figure 4 Reverberating flow in VA (V2 extracranial) in case of
brain death.
The role of color duplex sonography in the brain death 365
systolic velocity, the index of Gosling, volumetric flow rate
are more unsteady than qualitative ones and in patients with
BD depend generally on two factors — level of systolic blood
pressure and intracranial pressure during the investigation
[6,14—16]. Although there are some reports that showed
that a decrease in the total volume of cerebral blood flow
below 100 ml/min is in line with 100% mortality [17,18].
As it was shown in our study, the combination of intracra-
nial and extracranial tests increased the sensitivity of the
study up to 100%. The sensitivity of isolated transcranial
color duplex scanning was lower and depended on the time
when the test was carried on in patients who had their
clinical symptoms developed. The maximum sensitivity was
90% when the test was performed in the early period and
decreased to 80% when the investigation was done 6 h after
the symptom manifestation.
In addition, another factor which makes difficulty in
interpretation of ultrasound data is previous extensive
resection craniotomy in neurosurgical patients. In this case,
the intracranial pressure is usually much lower. Here TCD is
supposed to prolong the period when diagnosis of BD will be
established. Although in any case, the typical ultrasound pic-
ture of circulatory blood arrest is developed with the lapse
of time [19].
Cerebral angiography remains a ‘‘gold standard’’ of
diagnostics in angiology. It should be noted that in cases
with craniotomy, even when cerebral angiography was per-
formed, there is flow of contrast into the cranial cavity,
which makes the interpretation of the clinical data difficult
[20—23].
BD is a clinical diagnosis and any confirmatory tests are
auxiliary. The diagnosis of BD cannot be based only on confir-
matory tests and neurologic criteria assessment is required.
Conclusions
CDS of patients with BD reveals oscillating flow or systolic
spikes in distal ICA, VA, intracranial vessels and spontaneous
echo contrast in proximal ICA. In TCD, the most common
finding is MCA with reverberating flow. There are some diffi-
culties in detection of basilar system and it depends on the
time of BD manifestation.
The optimum combination is extracranial and intracranial
scanning in the early stages of BD.
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