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Vascular

Transcranial Doppler Sonography


Pulsatility Index (PI) Reflects
Intracranial Pressure (ICP)
Johan Bellner, M.D.,* Bertil Romner, M.D., Ph.D.,* Peter Reinstrup, M.D., Ph.D.,*
Karl-Axel Kristiansson, M.L.T.,† Erik Ryding, M.D., Ph.D.,† and
Lennart Brandt, M.D., Ph.D.†
*Department of Neurosurgery, Department of Anesthesiology & Intensive Care and
†Department of Neurophysiology, University Hospital of Lund, Lund, Sweden

Bellner J, Romner B, Reinstrup P, Kristiansson K-A, Ryding E, CONCLUSIONS


Brandt L. Transcranial Doppler sonography pulsatility index (PI) Independent of the type of intracranial pathology, a
reflects intracranial pressure (ICP). Surg Neurol 2004;62:45–51. strong correlation between PI and ICP was demonstrated.
Therefore, PI may be of guiding value in the invasive ICP
BACKGROUND
placement decision in the neurointensive care
In patients with intracranial pathology, especially when
patient. © 2004 Elsevier Inc. All rights reserved.
comatose, it is desirable to have knowledge of the intra-
cranial pressure (ICP). To investigate the relationship KEY WORDS
between ICP and transcranial Doppler (TCD) derived pul- Transcranial Doppler, pulsatility index, intracranial pres-
satility index (PI) in neurosurgical patients, a prospective sure, head injury, subarachnoid hemorrhage.
study was performed on patients admitted to our neu-
rointensive care unit.
METHODS ranscranial Doppler sonography (TCD) was
Daily TCD mean flow velocity (mFV) measurements were
made. TCD measurements were routinely performed bi-
T primarily established as a sensitive method
for detection of changes in cerebral blood flow ve-
laterally on the middle cerebral artery (MCA). PI (peak
systolic-end diastolic velocities/mean flow velocity) was locities in patients with aneurysmal subarachnoid
calculated. hemorrhage (SAH) indicating vasospasm [2]. The
RESULTS TCD technique is noninvasive and can easily be
Eighty-one patients with various intracranial disorders repeated bedside without any risk for the patient.
who had an intraventricular catheter for registration of The agility of the TCD equipment has also raised
the ICP were investigated: 46 (57%) patients had sub- hopes for ultra early assessment of intracranial dy-
arachnoid hemorrhage, 21 (26%) patients had closed namics following head injury [13]. The value of TCD
head injury, and 14 (18%) patients had other neurosurgi- recordings in patients with head injury is, however,
cal disorders. A total of 658 TCD measurements were
controversial even though changes in flow veloci-
made. ICP registrations were made parallel with all TCD
measurements. A significant correlation (p ⬍ 0.0001) was ties may enable early detection of potentially treat-
found between the ICP and the PI with a correlation able cerebral blood flow (CBF) disturbances.
coefficient of 0.938: ICP ⫽ 10.93 ⫻ PI – 1.28. In patients with intracranial pathology, especially
In the ICP interval between 5 to 40 mm Hg the correla- when comatose, it is often paramount to have con-
tion between ICP and PI enabled an estimation of ICP from tinuing knowledge of the intracranial pressure
the PI values with an SD of 2.5. The correlation between (ICP). Exact ICP measurement is obtainable only by
the cerebral perfusion pressure (CPP) and PI was signif-
an invasive intracranial pressure device [7,11].
icant (p ⬍ 0.0001) with a correlation coefficient of ⫺0.493.
When separating the measurements in severely elevated However, a relationship between ICP and the pul-
(⬎120 cm/s) and subnormal (⬍50 cm/s) TCD mFV values, satility index (PI) in head injured patients has been
the correlation coefficient between ICP and PI was 0.828 described [8,14]. These findings have been further
(p ⬍ 0.002) and 0.942 (p ⬍ 0.638), respectively. evaluated in an experimental mathematical model
[21]. No prospective study on the possible relation-
ship between ICP and PI has, to our knowledge,
Address reprint requests to: Johan Bellner, M.D., Department of Neu-
rosurgery, University Hospital, S-221 85 LUND, Sweden.
been performed on patients with intracranial pa-
Received June 6, 2001; accepted December 15, 2003. thology equipped with intraventricular ICP moni-
© 2004 Elsevier Inc. All rights reserved. 0090-3019/04/$–see front matter
360 Park Avenue South, New York, NY 10010 –1710 doi:10.1016/j.surneu.2003.12.007
46 Surg Neurol Bellner et al
2004;62:45–51

toring. Presently, such a study was carried out on Kolmogorov-Smirnof’s test. An estimated ICP from
the postulation that increased ICP is paralleled by PI was determined from the regression equation.
an increase in PI. The validity of the TCD(PI) method for ICP measur-
ing was tested by a Bland & Altman plot [3]. Sensi-
tivity and specificity for ICP(PI) were calculated in
Materials and Methods the ICP range of 0 to 20 and 0 to 40 mm Hg.
PATIENT POPULATION
Eighty-one patients were included with the follow-
ing types of intracranial disorders, verified by com- Results
puterized tomography (CT): 46 (57%) had aneurys- Eighty-one patients (37 males and 44 females) aged
mal subarachnoid hemorrhage, 21 (26%) severe 2 to 79 years (mean 52 years) were investigated
head injury, 7 (9%) spontaneous intracerebral hem- daily with a total of 658 PI measurements. The pa-
orrhage, and 7 (9%) had other neurologic disorders tients had a mean (⫾ SD) arterial partial pressure of
[encephalitis (n ⫽ 1), meningitis (n ⫽ 3), meningi- carbon dioxide (PCO2) of 4.84 ⫾ 0.64 (range 3.25–
oma (n ⫽ 1), idiopathic intracranial hypertension (n 7.5) kPa, a heart frequency of 79 ⫾ 17 (range 47–
⫽ 1), and sagittal sinus thrombosis (n ⫽ 1)]. 142), 97.3% with regular sinus rhythm, and a mean
INTRACRANIAL PRESSURE arterial blood pressure (MAP) of 92 ⫾ 16 mm Hg
MONITORING (range 48 –162) at the time of investigation.
The correlation between the cerebral perfusion
All patients received an intraventricular catheter
pressure (CPP) and PI was significant (p ⬍ 0.0001)
for continuous recording of the intracranial pres-
with a correlation coefficient of ⫺0.493 (Figure 1).
sure (HanniKath, 7F, pvb Medizintechnik Gmbh &
This finding was paralleled by a similar significant
Co. kg, Kirchseeon, Germany).
correlation (p ⬍ 0.0001) between CPP and ICP
TCD where the similar correlation coefficient was
One investigator conducted all TCD examinations. ⫺0.477.
TCD measurements were performed parallel to the In the overall results there was a significant cor-
ICP registration. relation (p ⬍ 0.0001) between the ICP and the PI
The daily TCD measurements were conducted with a correlation coefficient of 0.938 (Figure 2).
transtemporally using a traditional 2-MHz trans- When separating severely elevated (⬎120 cm/s)
ducer (EME TC-64 Eden medical records, Uberlin- and subnormal (⬍50 cm/s) TCD mFV values, the
gen, Germany). The TCD measurements were rou- correlation coefficient between ICP and PI was 0.828
tinely performed bilaterally on the middle cerebral (p ⬍ 0.002) and 0.942 (p ⬍ 0.638 because of a low
artery (MCA). Recordings were documented on a number of measurements), respectively (Figures 3
videographic printer for later analysis (Sony VP and 4). Only in one of 658 measurements (0.15%),
850). The depth and angle of insonation giving the the mFV exceeded 120 cm/s in conjunction with an
highest mean flow velocity (mFV) in MCA was al- ICP above 20 mm Hg (Figure 3). However, only in the
ways chosen. Normal mFV in MCA was defined as 62 ICP interval 5 to 40 mm Hg were the data normal
⫾ 12 cm/s [1]. Consequently, mFVs were consid- distributed around the regression line. Omitting re-
ered subnormal when below 50 cm/s and supernor- peated measurements, and only considering the ini-
mal when above 74 cm/s. mFVs above 120 cm/s tial TCD-ICP recording in each subject (n ⫽ 81) for
were considered severely elevated indicating vaso- the interval, 5 to 40 mm Hg R2 was 0.733 (p ⬍ 0.0001)
spasm or hyperemia [2,16]. Normal values for PI are with a SD 2.5. The regression line is ICP(PI) ⫽ 11.1
0.7 ⫾ 0.3 [20]. ⫻ PI – 1.43. Using the regression equation we get
ICP(PI) ⫽ ICP ⫾ 2.5 (SD) with a 95% confidence
CALCULATIONS AND STATISTICAL interval of ⫾4.2.
METHODS A Bland and Altman plot of all measurements
PI was calculated according to the method of Gos- confirmed that the difference between the observed
ling [6]. PI is derived from the difference in the ICP and the ICP predicted from the PI was within the
systolic and diastolic flow velocity divided by the ⫾4.2 of the observed ICP (Figure 5).
mFV. In an ICP span between 0 and 20 mm Hg, the
The PI data were correlated to ICP and CPP and method had for all measurements a sensitivity of
the correlation coefficient calculated. To control 0.88 and a specificity of 0.69, and for the first mea-
the linear correlation, the residuals were tested for surement only a sensitivity of 0.91 and a specificity
normal distribution around the regression line with of 0.79, for detecting an ICP ⬎10 mm Hg. To detect
Pulsatility Index Reflects Intracranial Pressure Surg Neurol 47
2004;62:45–51

Graph demonstrating a significant correlation between the CPP and PI with a correlation coefficient of ⫺0.493 (p
1 ⬍ 0.0001) and a correlation formula of: CPP ⫽ 89.646 – 8.258 ⫻ PI. The correlation between CPP and PI is mainly
when PI ⬎3. The dotted lines are the 95% confidence interval for the regression line, which can be significantly affected
by outliers when PI is large.

an ICP ⬎ 20 in a population with ICP between 10 and and not true volume flow, has triggered further
40, the method had for all measurements a sensi- development in the utilization of acquired data
tivity of 0.83 and a specificity of 0.99, and for the from the TCD investigations.
first measurement only a sensitivity of 0.89 and a In neurointensive care, knowledge of ICP is often
specificity of 0.92. essential. When measuring ICP the use of an intra-
ventricular catheter has for decades been consid-
ered as gold standard [11].
Discussion In the present study, we found independent of
TRANSCRANIAL DOPPLER IN intracranial pathology, a significantly strong posi-
NEUROINTENSIVE CARE tive correlation between PI and intraventricular ICP
The mobility of the equipment, the possibility of monitoring. Notably, the correlation was still strong
repeated bedside investigations together with the in the patient subgroup demonstrating mFV values
noninvasive nature of the technique, makes TCD above and below normal interval.
measurements attractive in the attempt to estimate A less clear correlation (⫺0.493) between PI and
CBF in acute care settings. The basic technical lim- CPP was seen. In head injured patients, Chan et al
itation, i.e., measuring cerebral blood flow velocity [4], reported a correlation (⫺0.725) between PI and

Graph demonstrating a significant correlation between the ICP and the PI with a correlation coefficient of 0.938 (p
2 ⬍ 0.0001) and a correlation formula of: ICP ⫽ 10.927 ⫻ PI – 1.284. The dotted lines are the 95% confidence interval
for the regression line, which can be significantly affected by outliers when PI is large.
48 Surg Neurol Bellner et al
2004;62:45–51

Graph demonstrating a significant correlation between the ICP and PI in measurements when TCD mFV exceed 120
3 cm/s. The correlation coefficient between ICP and PI was 0.828 (p ⬍ 0.002). The dotted lines are the 95% confidence
interval for the regression line, which can be significantly affected by outliers when PI is large.

CPP with an even better correlation (⫺0.942) as increases. Consequently, the TCD-PI measurement
CPP decreased below a critical value of 70 mm Hg. gives a fairly good estimation of the ICP, which
In an experimental mathematical model study, might be of value in unconscious patients.
Ursino et al [21], described relationships between
perfusion pressure, autoregulation and TCD wave- PI IN ANEURYSMAL SUBARACHNOID
form during various settings in cerebrovascular he- HEMORRHAGE
modynamics. These theoretical models indicate The correlation between ICP and PI was still intact
that during normoventilation within normal blood in SAH patients suffering vasospasm detected by
pressure range, sudden increases in PI are only TCD (Figure 3). Cerebral vasospasm in SAH is char-
attainable with a rise in ICP. Our clinical results are acterized by a high mFV through the vasospastic
in agreement with these findings. However, to rely artery, often exceeding 120 cm/s [2]. In such cases
on PI in daily practice one has to determine the there will be a decrease in CBF because of an in-
sensitivity and specificity of the method. In the crease in cerebrovascular resistance through the
acceptable ICP interval of 0 to 20 mm Hg, the TCD is artery [17]. The high flow velocity is only obtain-
highly sensitive with a medium high specificity. In able if the peripheral vascular resistance remains at
the supranormal ICP range between 10 and 40 mm a relatively low level. As a result a high mFV is
Hg the sensitivity decreases while the specificity usually not found in patients with high ICP as they

Graph demonstrating the correlation between the ICP and PI in measurements with TCD mFV below 50 cm/s. The
4 correlation coefficient between ICP and PI was 0.942 (p ⬍ 0.638). The dotted lines are the 95% confidence interval
for the regression line, which can be significantly affected by outliers when PI is large.
Pulsatility Index Reflects Intracranial Pressure Surg Neurol 49
2004;62:45–51

lation between ICP and PI (R2 ⫽ 0.69) was found. In


severe head injured patients, Martin et al [12] re-
ported significantly higher PI values on Day 0, com-
pared to Days 1 through 3 and Days 4 through 14
post-trauma. These findings strongly suggest the
presence of high distal vascular resistance in the
early phase after head injury. The authors also
showed that one-third of patients with severe head
injuries have vasospasm, and that vasospasm will
significantly change both mFV and PI. In our study
we found that PI reflected ICP even when mFV was
above 120 in the ICP range of 0 to 20 mm Hg, but
In the ICP interval 5 to 40 mm Hg was the data with only one reading above 20 mm Hg.
5 normal distributed around the regression line. The With data obtained by TCD, Czosnyka and asso-
correlation formula in this interval is: ICP(PI) ⫽ 11.5 ⫻ PI ciates [5] made estimations of CPP after head injury
– 2.23 and R2 ⫽ 0.732, p ⬍ 0.0001. Using the regression and concluded that such measurements may be of
equation we get ICP(PI) ⫽ ICP ⫾ 2.5 (SD) with a 95%
confidence interval of ⫾4.2. The Bland and Altman plot value in situations where direct measurements of
confirmed that 95% of the ICP (PI) data are within the CPP are not readily available. Moreno et al [14]
⫾4.2 limit Bland and Altman plot showing ICP(PI)-ICP and found a positive correlation of 0.60 between PI and
mean ICP. CPP. This correlation is probably dominated by the
ICP. In our experience, reduced mFV after head
injury always indicates reduced volume flow in the
have a concomitant increase in small vessel resis- insonated artery, and can hence be helpful to indi-
tance [9]. In the present study, only once in 658 cate compromised cerebral perfusion, and a low
measurements was an mFV exceeding 120 cm/s ob- mFV postinjury should guide the choice of blood
served in conjunction with an ICP above 20 mm Hg pressure targets that should be used during the
(Figure 3). cerebral resuscitation [16]. An example of this is
our findings of frequently reduced mFV in measure-
PI IN HEAD INJURY ments where ICP exceeded 20 mm Hg with a corre-
With repeated carotid Doppler sonograms, Steiger sponding rise in PI.
[19] investigated PI in patients with severe head
injury as compared to healthy volunteers. This ex- PI IN HYDROCEPHALUS
tracranial utilization of PI revealed values between In hydrocephalic children a decrease of PI in the
1.5 to 2.0 in control subjects with a gradual increase postshunting test as compared with the preshunt-
in cases with posttraumatic brain edema. PI values ing test has been shown [15]. Furthermore, after
⬎3 were associated with severe intracranial hyper- endoscopic third ventriculostomy for the treatment
tension, and in cases of angiographically demon- of obstructive hydrocephalus, pre- and postopera-
strated cerebral circulatory arrest, PI values in the tive PI measurements have been shown useful for
range of 6 to 8 were found. evaluation of fenestration patency [22]. Recently,
Presently a significant correlation between PI and the value of PI measurements was confirmed in a
ICP was found, the correlation being stronger as study of 21 hydrocephalic patients [18].
compared to previous studies. Homburg et al [8],
investigated 10 head injured patients and demon- FACTORS THAT INFLUENCE PI
strated a positive exponential correlation between Flow velocity, the velocity pattern, and thereby the
PI and the epidural pressure (r ⫽ 0.82). McQuire PI may be influenced by different factors, like hemo-
and colleagues [13] performed TCD measurements dynamic, respiratory, and hematologic parameters,
within 3 hours after injury on 22 head injured pa- and, in the case of brain vessels, tissue compliance.
tients. Thirteen of the patients had either computed For this reason, the absolute value of this index is,
tomography verified space-occupying hematomas in general, not considered sufficient to characterize
or brain swelling. Among these cases 10 had an overall intracranial hemodynamic conditions if no
increased PI in this ultra-early phase. Recently, other information is simultaneously provided. The
Moreno et al [14] correlated TCD measurements main advantage of PI is that, being a ratio; it is not
with ICP and CPP values in 125 patients with severe affected by the angle of insonation.
head injury. They found that an elevated PI predicts The arterial pressure in large and medium sized
poor outcome (PI 1.56), and furthermore, a corre- cerebral arteries is only slightly reduced compared
50 Surg Neurol Bellner et al
2004;62:45–51

to the pressure created by the heart, but in the changes in cerebral perfusion pressure upon middle
arterioles the normal mean pressure drops. During cerebral artery blood flow velocity and jugular bulb
venous oxygen saturation after severe brain injury.
elevated intracranial pressure, the arterioles are
J Neurosurg 1992;77:55–61.
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cular resistance reducing the flow, and thereby, the Pickard JD. Cerebral perfusion pressure in head-
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elevation of PI in diabetic patients with cerebral nial Doppler recordings in raised intracranial pres-
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11. Lundberg N. Continuous recording and control of
The flow velocity pattern in cerebral arteries is ventricular fluid pressure in neurosurgical practice.
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In a situation with severely raised ICP one might acterization of cerebral hemodynamic phases follow-
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Conclusion method of assessing intracranial pressure in hydro-
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Our data shows a highly significant correlation be- 16. Romner B, Bellner J, Kongstad P, Sjöholm H. Elevated
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COMMENTARY applicability significantly. However, as the authors
Bellner et al have added to the growing body of point out, I think it could be a useful technique in
knowledge regarding transcranial Doppler sonogra- patients in whom elevated intracranial pressure
phy and its use in various neurosurgical clinical was suspected or in those patients in whom it
problems. This study has the advantage of being would be important to exclude.
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of the technique in several different pathologies, it Professor of Neurosurgery
is important to realize that the intracranial dynam- University of Minnesota
ics and the cause of increased intracranial pressure Minneapolis, Minnesota

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