Application of transcranial Doppler ultrasound in pediatric patients

Application of transcranial Doppler ultrasound in pediatric patients

Praca O R Y G I N A L N A / original article
Application of transcranial Doppler ultrasound in pediatric patients:
how to verify the indications?
Wykorzystanie przezczaszkowych badań naczyn mózgowych metodą Dopplera u pacjentów
pediatrycznych: jak zweryfikować wskazania?
Ilona Kopyta1, Ewa Emich-Widera1, Maciej Świat2, Anna Gołba3
Department of Neuropediatrics, Medical University of Silesia, Katowice,
Department of Neurology, Medical University of Silesia, Katowice
3
Neurological Department, Upper-Silesian Medical Center, Katowice
1
2
STRESZCZENIE
ABSTRACT
The transcranial Doppler (TCD) is the diagnostic procedure
commonly used in ambulatory and hospital practice. As the
method does not expose the patients to the X-ray radiation
and does not require the anesthesia, it becomes more and
more common, especially in children. According to the
American Academy of Neurology the value of TCD is well
established in sickle cell disease for assessing stroke risk, in
monitoring the vasospasm after subarachnoid hemorrhage
and in diagnosing right-to-left cardiac shunts (Evidence Type
A Class I-II). The usefulness of TCD in intracranial steno-
Celem pracy jest identyfikacja najistotniejszych wskazań do
przeprowadzenia badań naczyń mózgowych metodą Dopplera
u dzieci. Materiał, metoda. Badaniem objęto 140 pacjentów
w wieku od 8 miesiąca do 18 roku życia (93 dziewczynki i 47
chłopców). Wskazaniami do hospitalizacji w Klinice Neurologii Wieku Rozwojowego były: bóle głowy, omdlenia, zawroty
głowy, udar niedokrwienny potwierdzony badaniami neuroobrazowymi. U wszystkich pacjentów przeprowadzono badanie fizykalne i neurologiczne, a także przezczaszkowe badanie naczyń
mózgowych metodą Dopplera oraz magnetyczny rezonans
jądrowy mózgu (ang. Magnetic resonance imaging); w przypadku podejrzenia malformacji naczyniowej wysuniętego na
podstawie badania TCD (ang. Transcranial Doppler) dodatkowo
wykonywano angiografie rezonansu magnetycznego. Wyniki.
Na podstawie przeprowadzonej diagnostyki rozpoznano: napięciowe bóle głowy u 52 dzieci, migrenę u 14, wtórne bóle głowy
u 36, udar mózgu u 38. Nieprawidłowe wyniki TCD stwierdzono
u 50 dzieci: u 10 z nich wynik sugerował hypoplazję naczyniową; w tejże grupie potwierdzono hypoplazję tętnicy kręgowej u 4 dzieci. U 38 dzieci z udarem niedokrwiennym mózgu
obserwowano ewolucję od cech stenozy naczynia objętego
patologią do częściowej lub pełnej rekanalizacji. Wnioski.
Badanie przepływów naczyń mózgowych metoda Dopplera jest
szczególnie przydatne do śledzenia ewolucji zmian przepływu
krwi u dzieci z udarem niedokrwiennym mózgu. U większości
pacjentów z bólami głowy nie stwierdzono nieprawidłowości w
parametrach przepływu krwi.
Słowa kluczowe: przezczaszkowe przepływy krwi metodą
Dopplera, dzieci, bole glowy, udar niedokrwienny, wskazania
Vol . 1 9 /20 1 0 , n r 3 7
Aim. The aim of the study is to identify the most important
indications for the transcranial Doppler in pediatric patients.
Material, method. The study population consisted of 140 children aged 8 months to 18 years (93 girls, 47 boys). The indications for the patients’ admittance were: headache, vertigo,
syncope, stroke confirmed by the brain computed tomography.
All the patients were examined physically and neurologically;
the transcranial Doppler and the head MRI were performed. In
the cases were cerebrovascular malformation was suspected,
the magnetic resonance angiography was conducted. Results.
According to the clinical examination and the neuroimaging
we diagnosed: tension headache in 52 children: migraine in
14 children; the symptomatic headache in 36 children: and
the ischemic stroke in 38 children. The pathological result of
the TCD was found in 50 children: in t10 of them the result
suggested the hypoplasia of intracranial vessels; in the same
group in 4 children the vertebral artery hypoplasia was confirmed. In 38 children with ischemic stroke the evolution of the
blood flow, from stenotic signs to partial/ full recanalization,
was observed. Conclusions. The TCD is extremely important in
the blood flow evolution investigation of the pediatric ischemic
stroke patients. In majority of children with headache no TCD
pathology was found.
Key words: transcranial Doppler, children, headache, stroke,
indications
33
Praca O R Y G I N A L N A / original article
I. Kopyta, E. Emich-Widera, M. Świat et al.
occlusive disease is less evident but still it is considered as
useful for the detection of intracranial stenosis/occlusion or
detection of impaired cerebral hemodynamics in patients
with extracranial stenosis/occlusion and with cerebral smallartery disease (Evidence Type B, Class II-III) [1].
Although the headaches are not the indication for TCD
but in every-day practice the method is being commonly
used to provide information about cerebral hemodynamics
[2]. The clinical application of TCD remains to be determined. The aim of the study was to identify the most important indications for the transcranial Doppler in pediatric
patients.
city with coexisting turbulent character of the blood flow.
To assess cerebrovascular response to CO2 changes vessel
reactivity test with hyperventilation was performed. Mean
flow velocity between 2 measurements: under maximal
hyperventilation and hypoventilation were compared.
A relative difference higher than 15% argues against a
relevant impairment of cerebrovascular response [4].
All the TCD examinations were performed in conscious
children, without any signs of infection. The provocation
by hyperventilation was used in cooperative children, not
in the stroke children. The statistical analysis was performed with the exact Fisher’s test.
MATERIAL AND METHODS
RESULTS
The study population consisted of 140 children aged 8
months to 18 years (93 girls, 47 boys). All the patients were
hospitalized in the Neuropediatric Department within the
period of the last three years, the stroke patients within the
last 8 years. The indications for the patient’s admittance
were: headache, vertigo, syncope, ischemic stroke. All
stroke cases were confirmed with the brain computed tomography and/ or magnetic resonance imaging (MRI). The
neuroimaging (MRI and/ or MRA) was performed with 1,
5 Tesla machine and interpreted by an experienced pediatric radiologist. Some of the children required the general
anesthesia for the examination. All patients were examined
physically and neurologically; the transcranial Doppler and
the head MRI were performed in all of them. In the cases
were cerebrovascular malformation in TCD was suspected
the magnetic resonance angiography was conducted. The
TCD in the patients with headache/ vertigo and syncope was
performed in the interictal period; in the stroke patients- in
the acute state of disease.
The neurological state of the majority of examined
patients was normal, even of the thirty eight patients with
stroke. In the last group hemiparesis and /or facial nerve
paresis contralateral to the brain lesion was found.
The TCD examination was performed with single-channel portable unit Pioneer TC 2000 (EME Eden Medizinische Elektronik, Uberlingen, Germany) with a hand-held
transducer operated in a range-gated, pulse-waved mode
at 2MHz. Intracranial arteries were insonated through
the temporal window by use of standardized protocol[3].
Middle cerebral artery (MCA), anterior cerebral artery
(ACA), terminal segment of internal carotid artery (ICA)
and posterior cerebral artery (PCA) were examined. Arteries were distinguished by the position of the probe, the
depth of insonation and the direction of the blood flow.
The sample volume size was 8 to 10 mm in the axial and 5
mm in the lateral direction. The examined parameters of the
blood flow were: the mean blood flow velocity (MV), the
blood flow character (laminar or turbulent). The turbulent
blood flow was recognized when spectral broadening was
recorded. The features of the vessel stenosis were: increase
of the mean blood flow velocity (> 0,8 m/second) or the
blood flow velocity difference between the left and right
side (> 0,3 m/second) with coexisting turbulent character
of the blood flow. The vessel hypoplasia was diagnosed
when there was a significant decrease in blood flow velo34
The stroke patients were analyzed within the group 1.
According to the clinical data stroke patients were classified
as PACI (partial anterior circulation infarct, 11 children),
LACI (lacunar anterior circulation infarct, 7 children) and
TACI (total anterior circulation infarct, 2 children). According to the clinical and additional examinations and the International Headache Classification in most of the examined
patients the idiopathic headache was diagnosed (66 patients;
47, 1%); the group was divided into subgroup with tension
headache (52 children, 37, 1%, group 2) and migraine (14
patients, 10%, group 3). Secondary headache was found in
about 1/3 of the whole group (36 patients, 28, 5% - group 4)
(Table I). The positive family history (headaches in parents
and/or child’s siblings) was found in six children - four with
tension headache and two with migraine.
The pathological result of the TCD was found in 39
children (28% of all groups).
Table I. Examined groups of patients according to diagnoses
Group
Diagnosis
Number of patients
(total n=140)
1
Ischemic stroke
38
2
Tension headache
52
3
Migraine
4
- common
5
- classical
4
- benign paroxysmal vertigo
5
Symptomatic (total number 36
patients)
- Sinusitis/ tonsillitis
28
- Arachnoid cyst
4
- Instability/ hyperlordosis of
cervical vertebral column
2
- Glaucoma
2
Generalized increase of the blood flow velocity was
found in 19 patients with stroke and 10 patients with
migraine whereas in none in other groups (Table II). Vessels reactivity test was positive in four patients with classical migraine (group 3). Decrease of the segmental blood
flow velocity with turbulent blood flow was found in 10
Neurologia D ziecięca
Wykorzystanie przezczaszkowych badań naczyn mózgowych metodą Dopplera u pacjentów pediatrycznych: jak zweryfikować wskazania?
Table II. The statistical analysis of the TCD parameters within the examined patients
Parameter
Gr. 1
stroke
(N=38)
Gr. 2
Gr. 3
Tension headache Migraine
(N=52)
(N=13)
Gr. 4
Symptomatic
headache
(N=36)
Statistical significance
between the examined groups
of patients
(Fisher’s exact test)
Generalized
increase of blood
velocity
19
(50,0%)
0
(0,0%)
10
(76,9%)
0
(0,0%)
Gr.1-Gr.2: p<0,00001
Gr.1-Gr.4: p<0,00001
Gr.3-Gr.2: p<0,00001
Gr.3-Gr.4: p<0,00001
Turbulent blood
flow
15
(39,5%)
10
(19,2%)
0
(0,0%)
0
(0,0%)
Gr.1-Gr.2: p=0,05
Gr.1-Gr.3: p=0,006
Gr.1-Gr.4: p<0,00001
Gr.2-Gr.4: p=0,005
Segmental blood
velocity decrease
0
(0,0%)
10
(19,2%)
0
(0,0%)
0
(0,0%)
Gr.2-Gr.1: p=0,004
Gr.2-Gr.4: p=0,005
patients with tension headache (group 2). In 4 of them
vertebral artery hypoplasia was confirmed in the magnetic resonance angiography. Turbulent blood flow was also
found in 15 stroke children (group 1). The localization of
the blood vessel pathology was contralateral to the neurological deterioration found in the patient. Segmental blood
flow decrease was found in 10 cases only in the group with
tension headache (group 2) (Table II).
DISCUSSION
In the adult patients with tension headache and the healthy
ones no differences in TCD blood flow parameters were
found [5]. Moreover, in the adults with common migraine
and with classical migraine in the interictal period the TCD
parameters of cerebral vessels blood flow were similar to the
results in healthy ones [6,7].
In adolescents with migraine and tension headaches the
features of cerebral vessels hyperactivity was found only
during the headache incident. [8] Arjona et al. have examined the group of patients aged 16-50 years with migraine
and tension headache; the cerebral vessels hyperactivity
was found only in the patients with migraine[9].
In comparably large group of 133 children with headache examined by Maytal et al. (52% migraine, 21% tension headache, 19% unclassified headache) only 78 (59%)
underwent the neuroimaging (head CT and/ or MRI). Only
in 4 out of the 78 the pathological changes on neuroimaging were found. The authors did not perform the TCD
[10,11]. All the results mentioned above indicate that the
neuroimaging studies have a very limited value in the evaluating headaches in pediatric patients.
The huge group of 858 children aged from six months
to 18 years was examined by Hirsch et al.within the time of
seven years. The pathological findings in TCD were found
in 0, 4% (headache, orthostatic deregulation group), 5,4%
(acute neurological symptoms) and 22% of different reasons. The positive predictive value of finding any abnormaVol . 1 9 /20 1 0 , n r 3 7
lity was very low, so the indications for TCD performance
in children are very specific, for example the known other
vascular examinations of pathological processes of the
brain vessels (stenoses) and chronic diseases, like sickle
cell disease and angiitis [2]. Our results, however examinations not performed in such large group of patients, are
similar to the authors’. Moreover, the Fiermonte et al found
the increase of the blood flow in the migraine patients as
useful to differentiate between the diagnosis of migraine
and tension headache, which is also consistent with our
results [12]. Gergont A, Kozera G et al. results indicate,
that there are no specific features in the blood flow parameters between the children with migraine and tension headache, so the last and the largest group of pediatric patients
with headache, the tension headache group, still presents
the diagnostic problem[13,14]. As the pathophysiology of
migraine and tension headache is different, the TCD results
in the two groups are different as well. One of the features
specific to migraine is the blood vessel hyperactivity, confirmed also in our patients.
Nesterovskij et al. examined 140 children aged 6 – 16
years, with different types of headaches; they found the
increase of blood velocity in all types of headaches when
compared to the control group [15].
In the very small group (four children) with the suspicion of vessel hypoplasia on TCD examination, the magnetic resonance angiography results confirmed the initial
diagnosis. In much larger group of children analyzed by
Bojinova V et al. group of 205 children aged 3-15 years
with different symptoms - stroke, transient ischemic attacks,
focal seizures) the intracranial vessel hypoplasia was found
in 63 of them, mainly with the use of MRI [16].
In our group of symptomatic headache (group 4) no
specific features of cerebral blood flow were found. It
seems to be the cause of headache in the group, as the children with intracranial pressure for hydrocephalus, tumors,
head trauma or neuroinfections present the cerebral blood
flow disturbances [17-20].
35
Praca O R Y G I N A L N A / original article
All the patients of the group 1, the stroke patients,
admitted to hospital with the symptoms of hemiparesis
and/ or facial nerve paresis of the same side of the body;
some of them with speech and consciousness disturbances.
On the base of the clinical course and the results of neuroimaging we qualified all of them to the one of the three
stroke types: PACI, LACI or TACI. At the hospital admittance TCD results presented the stenotic blood flow in the
intracranial part of ICA and/or MCA and/ or ACA with
the increased mean blood flow velocity in the vessel compared to the opposite, healthy vessel, and the features of
the turbulent blood flow spectrum. At the discharge form
hospital in 9 patients of the group 1 the normalization of
the mentioned parameters was observed, but still in the last
10 of them the stenotic blood flow was present. This is the
group of patients requiring special care and the systematic
TCD examinations.
It is obvious that the pediatric patients with sickle cell
diseases are at risk of ischemic stroke; that risk increases
with the increase of blood flow velocity and that is the
group of patients which requires the regular blood transfusions [21-25]. Although in the described group of stroke
I. Kopyta, E. Emich-Widera, M. Świat et al.
children there are no patients with sickle cell disease, but
still the necessity of the TCD follow-up in that group seams
to be clear.
We did not find in the Polish literature any article comparing the quality and the prevalence of the cerebral blood
flow in pediatric patients with headaches and/ or vertigo
and/ or autonomic deregulation to the healthy children corresponding for the age and sex. Such project is going to be
the authors’ next aim.
CONCLUSIONS
The TCD is valuable non-invasive and ray-free technique. It
is extremely important in the blood flow evolution investigation in the ischemic stroke patients, as the change in the
blood flow parameters may predict the recurrence of stroke.
In majority of children with headache no TCD pathology
was found. In relatively small group of pediatric patients
the TCD result suggests the intracranial vessel malformation and makes the clinicians perform magnetic resonance
angiography. More thorough trial with the group of healthy
children is necessary to establish the potential frequency of
CNS vessel pathology in pediatric population.
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The publication is supported with grant of Polish Ministry of Science, number of arrangement N406 047 31/0986
Correspondence:
Ilona Kopyta, Department of Neuropediatrics Medical University of Silesia, 40-752 Katowice, 16 Medykow Str., Poland,
e-mail: [email protected]
Vol . 1 9 /20 1 0 , n r 3 7
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