Determination of Brain Death With Use of Color

Duplex Scanning in the Intensive Care Unit Setting

Gary W. Lemmon, MD; Randall W. Franz, MD; Nancy Roy, RVT; Mary C. McCarthy, MD; James B. Peoples, MD

Objective: To determine if color flow duplex scanning sumed brain death.

(CFDS) can be used for rapid confirmation of presumed
brain death.
Design: Pilot cohort study comparison of CFDS with ra-
dionuclide cerebral scanning (RCS) as the criterion standard.
Results: CFDS correctly identified 16 of 24 patients as
brain dead, confirmed by RCS. Eight patients with brain
flow on RCS were also correctly identified by CFDS. Only
two of 24 patients survived their severe injuries.

Setting: Community-based level I trauma center inten- Conclusions: CFDS provides a uniform, cost-effective
sive care unit. diagnostic tool for rapid confirmation of clinical brain
death with 100% accuracy. Its use should complement
Patients: Twenty-four patients who satisfied criteria for RCS, given its rapid interpretation, portability, and eco-
presumed brain death. nomical assessment of presumed brain death.

Main Outcome Measure: Confirmation of pre- (Arch Surg. 1995;130:517-520)

From the Department of
Surgery, Wright State
University School of Medicine
(Drs Lemmon, Franz,
and Peoples), and
McCarthy,
the Neurovascular Laboratory,
Miami Valley Hospital
(Ms Roy), Dayton, Ohio.
Rapid
confirmation of brain
death following severe
head injury requires a
timely diagnosis because of
medical, legal, and eco¬
nomic implications.14 The current diag¬
nostic tests (electroencephalography,
brain-stem evoked potentials, dynamic
computed tomographic scanning, cere¬
bral angiography, and RCS) all have dis¬
crete limitations (Table). Electroencepha-
lographic monitoring is portable. However,
it may be inconclusive in patients with hy¬
pothermia or barbiturate use, and it can
be challenging to obtain an isoelectric trac¬
ing in a busy intensive care unit.5 There¬
fore, physician interpretation is not al¬
ways uniform.6,7 Brain-stem evoked
potentials can be misleading if cochlear or
auditory nerve damage is present.6,8 Ra-
dionuclide cerebral scanning may not be
accessible in every intensive care unit.
Scalp and facial perfusion may mask de¬
termination of brain-flow cessation.9,10
Quality control issues regarding reagent
use and timing of injection remain
critical variables.1113 More invasive pro¬
cedures, such as dynamic computed to¬
mographic scanning and cerebral angiog¬
raphy, are highly accurate but costly and
require transport of severely ill patients to
the radiology suite.9,10,1415
We have identified acutely ill pa¬
tients presumed brain dead (absent pu¬
pillary, corneal, and gag reflexes; no mo¬
tor response; positive apnea test result)
with continued cerebral perfusion by RCS
who eventually recovered from their neu¬
rologic injury (for example, prolonged
emergence from anesthesia in severely
traumatized patients). Institutional policy
requires a confirmatory test to establish the
diagnosis of brain death. Thus, the need
for a more rapid and cost-effective ap¬
proach for confirming brain death in the
intensive care unit of our level I trauma
center prompted an evaluation of the use¬
fulness of CFDS. Based on previous work
in our noninvasive laboratory (G.W.L., un¬
published results, 1992), strict criteria were
developed to assess the sensitivity and
specificity of CFDS in identifying brain
death. Following institutional review board
approval, extracranial vessel insonation
See Patients and Methods
on next page

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 Sixteen patients (67%) were found to have no ce¬
rebral blood flow by CFDS on initial evaluation. This find¬
PATIENTS AND METHODS ing was confirmed in all 16 by RCS. Eight patients (33%)
were found to have continued cerebral perfusion by CFDS.
In three (13%) of these patients, perfusion subse¬
Twenty-four patients with the presumptive diagnosis
of brain death (absent pupillary, corneal, and gag re¬ quently ceased, requiring serial RCS studies. Three pa¬
flexes; no motor response; positive apnea test result) tients (13%) later died of causes other than their brain
in the intensive care unit underwent 25 examina¬ injury. Two patients (8%) eventually recovered from their
tions using CFDS prior to radionuclide cerebral scan brain injury. No patient had loss of perfusion identified
(RCS). Institutional Review Board approval was ob¬ by RCS but not by CFDS. The sensitivity and specificity
tained prior to cohort study. An ATL-Ultra-Mark-9 Du¬ of CFDS and RCS were both 100% for correctly identi¬
plex Scanner with a 5-MHz linear array probe (Ad¬ fying loss of cerebral blood flow. Of the 16 patients (67%)
vanced Technologies Laboratory, Bothell, Wash) was identified early, seven (29%) went on to organ procure¬
used to obtain a range-gated, Doppler angle-
ment.
corrected signal of the common, internal, and exter¬
nal carotid and vertebral vessels bilaterally. Peak sys¬
tolic and diastolic velocities, end-diastolic flow, and
flow reversal, if present, were determined. Techni¬
cian and interpreter were masked as to the results of Although a number of diagnostic tests can confirm clini¬
RCS. Results of CFDS were then tabulated and com¬ cally suspected brain death, each has specific limita¬
pared with RCS, the criterion standard. All patients tions associated with its use. As identified in the Table,
were euvolemic and were receiving mechanical ven¬ cost and time
tilator support, with oxygen saturation greater than 90% performing each test can be critical fac¬
and a mean arterial pressure of 60 mm Hg or greater.
tors in achieving a timely diagnosis. The need for a more
The cause of severe brain injury, outcome, and organ rapid and cost-effective screening test for the confirma¬
tion of brain death prompted an evaluation of CFDS at
procurement were reviewed retrospectively.
our institution. Yoneda and others16 in 1974 identified a
to-and-fro movement or oscillating wave pattern within
the internal carotid arteries that was associated with a
single systolic spike and reverse flow. These findings were
Cost Comparison Analysis for Clinical Brain Death distinguishable from both normal and diseased internal
carotid artery wave patterns. In 1982, Kreutzer and col¬
Total Time, leagues17 developed a computer-assisted analysis of com¬
Diagnostic Test Cost, $ min Limitation
mon carotid artery velocity waveforms to determine brain
Brain-stem evoked 315 60 False-positive nerve death. The sensitivity was 100% and specificity was 92%
potentials damage
Color flow duplex 320 30 Technician dependent using waveform indices of systolic and diastolic veloci¬
scanning ties. There was no assessment of internal carotid or ver¬
Radionuclide cerebral 467 30 Short half-life, quality tebral artery response. Payen et al10 evaluated pulsed Dop-
scanning control
pler common carotid artery blood flow in 28 patients,
Electroencephalography 460 90 Affected by medication,
with 14 confirmed brain deaths. Using logistic regres¬
temperature, and
electrical interference sion analysis, they determined that blood flow less than
Dynamic computed 773 30 Transport hazards, 31.4 mL/min was indicative of brain death. Their deter¬
tomography monitoring mination was cumbersome, however, requiring two probes
Cerebral angiogram 1500 60 Transport hazards, to correct for angle and diameter determinations. Their
monitoring error rate was 5% to 12%. No internal carotid or verte¬
bral artery measurements were performed, and only one
side was assessed for each patient. Kirkham and col¬
was completed on 24 patients with a presumptive diag¬ leagues18 and Hassler and colleagues19 reported indepen¬
nosis of brain death prior to RCS confirmation. A total dently that end-diastolic velocity changes can be iden¬
of 25 examinations were performed. All scans were done tified with rising intracranial pressure and loss of cerebral
in the intensive care unit at the patient's bedside. Spec¬
perfusion pressure. Feri et al20 used transcranial Dop-
tral analysis was used to measure systolic and diastolic pler analysis of middle cerebral artery blood flow in 22
velocity. patients with brain death. Three of six wave patterns they
identified were uniformly associated with brain death.
RESULTS Based on this literature review, criteria were devel¬
oped in our noninvasive vascular laboratory to evaluate
Twenty-four patients met the criteria for severe brain in¬ the accuracy of CFDS for rapid determination of clinical
jury and suspected brain death. Their ages ranged from brain death:
14 to 84 years, with a mean of 35 years. Fifteen (63%)
were male and nine (38%) were female. Fifteen patients •
Dampened internal carotid and vertebral artery signal
(63%) sustained their head injury in a motor vehicle ac¬ with narrow systolic spiked waveform.
cident, three (13%) in a fall, three (13%) because of a • End-diastolic velocity at or below baseline.
gunshot wound, and three (13%) secondary to a cere- • Color flow reversal in the internal carotid and verte¬
brovascular accident (Figure 1). bral arteries.

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 Figure 1. Mechanism of severe brain injury (n=24). Mean Glasgow Coma
Scale score, 3.5 (range, 3 to 15).

Use of CFDS enabled rapid identification of flow rever¬

sal in the extracranial vessels, confirming visually what
Yoneda and colleagues identified in wave patterns in 1974.
Brain death produces characteristic waveforms that in¬
clude a sharp systolic spike and reversal of flow during

systole with loss of diastolic flow in both the internal ca¬

rotid and vertebral arteries (Figure 2). Flow reversal is
readily seen with color flow imaging. The rapid change
in color from red (toward the probe) to blue (away from
the probe) reflects directional change in blood flow dur¬
ing early and late systole. As intracranial pressure in¬
creases and cerebral perfusion decreases, systolic flow re¬
versal develops during late systole. This waveform appears
similar to a triphasic pattern characteristic of muscular
arterial beds with high resistivity. Further rises in intra¬
cranial pressure produce loss of diastolic flow, and only
systolic waveforms can be seen. Lack of end-diastolic ve¬
locity indicates complete cessation of any flow in the in¬
ternal carotid and vertebral arteries. Common carotid ar¬
tery diastolic flow continues to escape via the external
carotid artery. As the intracranial pressure approaches
the systemic arterial pressure, only a sharp systolic spike
exists, without flow reversal or diastolic wave reflec¬
tion. As stagnation develops, no signal can be identified
within the vessel. These wave patterns have been repro¬
duced by others2022 in transcranial investigations.
By adherence to strict criteria, we were able to cor¬
rectly predict which patients had continued cerebral per¬
fusion despite the appearance of brain death (absent pu¬
pillary, corneal, and gag reflexes; no motor response;
positive apnea test result). Two of eight patients sur¬
vived their severe neurologic injury. Both recovered from
prolonged shock under general anesthesia and multiple
operations. It is our belief that a confirmatory test is man¬ Figure 2. Color and spectral patterns of the common and internal carotid
datory for brain death under such conditions because a and vertebral arteries in brain death. A sharp, narrow systolic spike with
clinical examination is inadequate. Additionally, CFDS reversal of flow below the baseline is evident. Note the loss of the flow
correctly predicted clinical brain death in all 16 patients signal at end-diastole of the internal carotid and vertebral arteries.
Real-time visualization is easily demonstrated in both the internal carotid
in whom it was eventually confirmed by RCS. Each pa¬
and vertebral arteries bilaterally when brain death exists.
tient demonstrated characteristic waveforms (Figure 2)
with no end-diastolic flow in the internal carotid or ver¬
tebral arteries bilaterally. End-diastolic flow was pres¬
ent in the common and external carotid arteries because all patient groups, and rapid interpretation makes this
of continued perfusion of the face and scalp. test a valuable adjunct for critical decision making in the
Color flow duplex scanning is an excellent modal¬ timely diagnosis of brain death. With continued appli¬
ity the rapid determination of brain death in the in¬
for cation of strict criteria, CFDS is cost-effective, rapid, and
tensive care unit. Accessibility, uniform applicability to 100% accurate compared with RCS.

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 Accepted for publication January 31, 1995.
Presented the 1994 Annual Scientific Session of
at
the Western Surgical Association, Palm Desert, Calif, No¬
vember 13, 1994.
Reprint requests to WSU Department of Surgery, Mi¬
ami Valley Hospital, Suite 7000, 1 Wyoming St, Dayton,
OH 45409 (Dr Lemmon).
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J. L. Glover, MD, Royal Oak, Mich: Dr Lemmon and his as¬
sociates have demonstrated that duplex ultrasound can be used
to provide objective clinical data regarding brain death, and I
believe it is a very useful technique. Though it is an indirect
assessment, patterns of flow in the internal carotid and verte¬
bral arteries do indicate the vascular status of the intracranial
circulation, which in the case of brain death becomes one of
absent perfusion and very high resistance to inflow. These
changes account for the "spiked" appearance of the systolic por¬
tion of the Doppler flow signal and the absence of diastolic flow.
Similar results using these same criteria of resistive and non-
resistive flow waveforms were reported by a group from Cedars-
Sinai earlier this year. Were there any subjects with intracra¬
nial pathology, such as cerebral vasospasm without brain death,
who might be regarded as controls, studied to better evaluate
the specificity of the technique?
Regarding the technical aspects of duplex ultrasound, par¬
ticularly color Doppler imaging, it is very important to be aware
of any filtering of the Doppler signal, as is typically done to elimi¬
nate low-frequency "noise" from wall motion. If these filters
are set too high they will also eliminate low-velocity signals dur¬
ing diastole and could give a false-positive result. For ex¬
ample, Figure 2 shows no diastolic flow in the common ca¬
rotid, although there was probably some small amount going
into the external carotid. It is also important that the Doppler
waveform data be consistent in all vessels evaluated, particu¬
larly both internal carotid and vertebral arteries. Finally, color
Doppler imaging must be used with caution as it is prone to
artifacts; spectral Doppler displays are much more sensitive to
flow phenomena and are the only source of objective, quanti¬
tative data. Color is helpful, but it is not quantitative.
Do the authors see any role for the addition of transcra¬
nial Doppler studies (using the same duplex ultrasound equip¬
ment) to directly evaluate the middle cerebral and basilar ar¬
teries? Second, have you had the opportunity to do serial
examinations in patients who were resuscitated after anoxic
events, and, if so, how did changes in flow correlate with the
clinical course?
Dr McCarthy: We did study some patients with other in¬
tracranial pathology. As you noticed, initially in our study there
were 18 patients. We have since added several more, includ¬
ing three patients with cerebrovascular accidents. All of these
patients progressed to brain death. Regarding reversible changes,
two of the patients in our series demonstrated abnormal inter¬
nal carotid artery waveforms with reversible changes and sur¬
vived; both walked out of the hospital. All patients had fixed,
dilated pupils and absent brain-stem function at the time of the
exam. They were oftentimes being resuscitated from major
trauma and had received an anesthetic technique which con¬
sisted primarily of oxygen and neuromuscular blockade.
With the current technical limitations of transcranial Dop¬
pler studies, you may not be able to visualize the arteries within
the head and therefore may have a study which shows a false
positive for brain death, particularly in times of low flow, so
we have not relied a great deal on this at this time.
Finally, we did have one patient who had serial exams who
eventually evolved to brain death. We were able to monitor this
patient using this technique. This is one of the areas where Dop¬
pler will be particularly helpful because we can just bring the
unit up, screen them, and then take it back downstairs if the
patient is not brain dead. The early diagnosis of brain death
will greatly facilitate the availability of organs for recovery ear¬
lier in the patient's course.