Download Transcranial Doppler for detection of changes in ophthalmic artery

Transcranial Doppler for detection of changes in ophthalmic artery blood flow
TANG Si-meng，LI Qian, GAO Feng-ling, WANG Yan-ling, ZHAO Lu, WANG Kang, HUANG Ying-xiang and
GAO Li-xin
Department of Ophthalmology, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China(TANG
Si-meng, WANG Yan-ling, ZHAO Lu, WANG Kang, HUANG Ying-xiang and GAO Li-xin)
Department of Ophthalmology, Beijing Chuiyangliu Hospital, Beijing 100022, China(LI Qian)
Department of Neurology, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China(GAO Feng-ling)
Correspondence to: Dr. WANG Yan-ling, Department of Ophthalmology, Beijing Friendship Hospital, Capital Medical
University, Beijing 100050, China (Tel:86-10-63138611. Email: [email protected])
LI Qian,GAO Feng-ling and TANG Si-meng contributed equally to this study.
This study was supported by National Natural Science Foundation of China“Study on protective mechanism of the retinal
ganglial cell(RGE) of ocular ischemic syndrome(OIS)”（No.81173412）;Beijing Natural Science Foundation“Study on
correlation between the haemodynamic changes of ocular ischemic syndrome and Toll-like receptors signal pathway”
（No.7122046）; Capital Medical Academy of Key Laboratory Ophthalmology Open Research Topic “Study on injury
mechanism of the retinal ganglial cell(RGE)of ocular ischemic syndrome(OIS).”
Keywords: transcranial Doppler; ophthalmic artery; severe internal carotid artery stenosis or occlusion;
blood flow
Abstract
Background The ophthalmic artery is a main branch of the internal carotid artery. Severe internal carotid
artery stenosis or occlusion may not only affect the blood supply to the brain, but may also cause ophthalmic
artery insufficiency, leading to ocular ischemia. In this study, we observed the blood flow spectrum changes
of the ophthalmic artery in patients with severe internal carotid artery stenosis or occlusion through
transcranial Doppler examination and explored the clinical value of transcranial Doppler in ophthalmology.
Methods Sixty-six patients at Beijing Friendship Hospital with a diagnosis of severe stenosis or occlusion in
the initial portion of the internal carotid artery were included in this study. We used transcranial Doppler
examination to detect the blood flow spectrum, blood flow direction, and peak systolic velocity of the
ophthalmic artery and compared the findings with those of the normal control group. Statistical analysis was
performed using a two-sample t-test.
Results Among the 66 patients, 4 had a normal ophthalmic artery blood flow spectrum, 27 had a
low-velocity ophthalmic artery blood flow spectrum, 27 had a reverse and low-pulsation ophthalmic artery
blood flow spectrum, and 8 did not undergo measurement of their ophthalmic artery trunk blood flow signal.
The ophthalmic artery blood flow direction was positive in 31 patients, and the peak systolic velocity was
significantly lower in these patients than in patients in the normal control group (P < 0.05). The ophthalmic
artery blood flow direction was reverse in 27 patients, and the peak systolic velocity in these patients showed
no significant difference from that in patients in the normal control group (P > 0.05).
Conclusion Transcranial Doppler allows for objective evaluation of hemodynamic changes in the
ophthalmic artery in patients with internal carotid artery stenosis, clarifying the blood supply of the eye, and
thus having clinical value in ophthalmology.
INTRODUCTION
The ophthalmic artery (OA) is a main branch of the internal carotid artery (ICA). Severe internal carotid
artery stenosis or occlusion may not only affect the blood supply to the brain, but may also cause OA
insufficiency, leading to ocular ischemia. Therefore, research on the hemodynamic changes in the OA in
patients with ICA stenosis or occlusion has attracted increasingly more ophthalmologists’ attention.1
Transcranial Doppler (TCD) is simple and noninvasive, has been widely used in the inspection of
cerebrovascular disease, and allows for judgment of the degree of stenosis of the intracranial and extracranial
vessels and collateral compensatory circumstances.2 However, there are few reports on assessment of the
blood supply characteristics of the OA by TCD. This study was performed to observe the blood flow
spectrum changes of the OA in patients with severe ICA stenosis or occlusion through TCD examination to
clarify the blood supply of the OA and explore the clinical value of TCD in ophthalmology.
METHODS
Patients
A total of 66 patients at Beijing Friendship Hospital with a diagnosis of severe stenosis (≥80%) or
occlusion in the initial portion of the ICA were included in this study between September 2010 and
December 2011. Forty-eight patients were male and 18 were female, with an age range of 53 to 72 years
(average, 62.6 ± 9.4 years). All diagnoses were confirmed by computed tomographic angiography, magnetic
resonance angiography, or digital subtraction angiography (Figure 1).
Forty individuals were included in the normal control group (20 male and 20 female patients; age,
52–70 years; average, 60.8 ± 8.6 years). All were confirmed to be healthy without arteriosclerosis or any
cardiovascular or cerebrovascular diseases.
Equipment and methods
We used German-made TCD ultrasonic diagnostic equipment according to the standard method to
detect the blood flow signal of the initial portion of the ICA with a 4-MHz probe and the blood flow signal of
the basicranial artery with a 2-MHz probe. We reduced the ultrasonic power to the minimum (17 mW) or
10% and set the detection depth at 50 mm, positioning the probe on the upward aspect of the eyelid with a
slight inward angle to determine the pulsation and direction of the distal blood flow of the OA necessary to
store the best distal blood flow signal (40- to 50-mm depth range). We then increased the depth to 55 to 65
mm to detect the blood flow signal of the ICA siphon inside the eye window and stored the two-way blood
flow signal or maximum flow rate signal at 60 to 62 mm (C3 segment or the siphon knee). We avoided
sampling deeply or positioning the probe to the upside with a slight angle to store the blood flow signal in
the front (C4 segment or the lower limb of the siphon) or behind (C2 segment or the upper limb of the siphon)
the probe.
At the same time, we closely observed the blood flow direction, frequency spectrum, and velocity of the
OA while paying attention to the collateral blood flow from the anterior communicating artery, posterior
communicating artery, and supraorbital artery. The TCD examination in all subjects was performed by the
same operator.
Statistical analysis
Results are given as mean ± standard deviation (SD). Differences between means were assessed using a
two-sample t-test with P < 0.05 considered statistically significant. The SPSS 17.0 statistical software
package was used (SPSS Inc., USA).
RESULTS
The TCD findings of the 66 patients with severe stenosis or occlusion in the initial portion of the ICA
were as follows: 4 patients had a normal OA blood flow spectrum (Figure 2), 27 patients had a low-velocity
OA blood flow spectrum (Figure 3), 27 patients had a reverse and low-pulsation OA blood flow spectrum
(Figures 4 and 5), and 8 patients did not undergo measurement of their OA trunk blood flow signal (only
some low-velocity and low-pulsation positive or reverse collateral blood flow was detected nearby).
The OA blood flow direction was positive in 31 patients, and the peak systolic velocity (PSV) in these
patients was (25.10 ± 7.02) cm/s, showing a significant difference from that in patients in the normal control
group (P < 0.05). The OA blood flow direction was reverse in 27 patients, and the PSV in these patients was
52.11 ± 24.30 cm/s, showing no significant difference from that in patients in the normal control group (P >
0.05) (Table 1).
DISCUSSION
With aging of the population and changes in dietary structures, the incidence of ICA stenosis induced
by atherosclerosis is increasing. Severe ICA stenosis or occlusion may not only lead to cerebrovascular
disease, but can also directly affect the blood supply to the eye. The main artery of the ophthalmic system is
the OA, also known as the first branch of the ICA, which is directly derived from the ICA siphon under the
siphon bed in most cases; however, it is rarely derived from the middle meningeal artery. Thus, in cases of
severe ICA stenosis or occlusion before the OA branch, OA insufficiency readily occurs, leading to ocular
ischemia.3
Ocular ischemia is the foundation of many eye diseases, such as amaurosis fugax, venous stasis
retinopathy, neovascular glaucoma, ischemic optic neuropathy, and ocular ischemia syndrome (OIS). OIS is
the most serious and easily misdiagnosed condition, causing increasingly more concern among
ophthalmologists. Many studies have shown that OIS is mainly due to long-term hypoperfusion of the OA,
resulting in diffuse retinal ischemia, and that it is closely related to persistent hemodynamic changes of the
ophthalmic vessels. Research on the hemodynamic changes of the OA can clarify the blood supply of the eye
and allow for exploration of the pathogenesis of ophthalmopathies associated with ICA stenosis, thus
providing guidance for early diagnosis of the disease.
TCD is simple and noninvasive, and has high clinical value for the diagnosis of extracranial and
intracranial artery stenosis. It has been widely used in the inspection of cerebrovascular disease. It not only
allows for judgment of the degree of stenosis of the extracranial and intracranial vessels, but is also sensitive
enough to evaluate the collateral circulation compensatory circumstances.1 It is mainly based on ultrasonic
Doppler detection of the dynamic changes in the hemodynamic and physiological parameters of the main
intracranial and extracranial arteries and on the blood flow velocity, allowing for assessment of the blood
flow condition and speculation of the corresponding changes in the blood flow volume to the local
vasculature. We previously examined the blood stream of the OA, focusing only on the degree of cerebral
ischemia and the state of the collateral circulation. Assessment included the anterior communicating artery of
the circle of Willis, the posterior communicating artery of the circle of Willis, and the OA to evaluate the
blood supply to the brain. However, less attention was given to objective evaluation of the hemodynamic
changes and blood supply of the OA. This study was performed to observe the blood flow spectrum changes
of the OA in patients with severe ICA stenosis or occlusion by TCD to analyze the regular hemodynamic
pattern of the OA and clarify the blood supply of the eye.
We found reversed OA blood flow in 27 patients (40.9%) with severe ICA stenosis or occlusion,
indicating that the blood flow through the external carotid artery–OA system to the ICA system has lower
resistance and presents the typical reverse low-pulsation spectrum. However, the PSV ranged from 21 to 110
cm/s; this is likely associated with differences in the reparative ability of the collateral circulation of the
circle of Willis and the adjustment ability of the vasculature itself. An increasing reverse flow velocity
indicates that the collateral circulation of the circle of Willis is insufficient and that the external carotid
artery–OA system is good; thus, the blood flow through the OA to the intracranial arteries rises, increasing
the intracranial blood supply and resulting in a decreased blood supply to the eye. This is in agreement with
Reinhard’s research,4 who considered that serious carotid artery stenosis must be accompanied by circulatory
disturbance of the cerebral arterial circle and uneven pressure; formation of collateral arteries of the eye
participate in the cerebral blood supply, which leads to ocular ischemia because of the blood flow reversal.
At this point, the body increases the blood flow velocity of the OA to increase the blood supply to the
intracranial arteries while also reducing the blood flow resistance to adapt to the continuous blood supply at
diastolic time to the requirements of the intracranial arteries. Both have an important significance to the
compensatory blood supply to the intracranial arteries in patients with severe ICA stenosis or occlusion. On
the other hand, the PSV of the OA with no reflux was significantly lower than that of the normal control
group in the present study, showing a low-velocity spectrum on TCD. This is in agreement with Zhangbin’s
report,5 who considered that in cases of severe ICA stenosis or occlusion, hemodynamic changes in the distal
artery and reduction of the PSV of OA are important mechanisms for the pathogenesis of OIS caused by the
ICA stenosis. However, the spectrum of the OA blood flow in four patients was normal in this study, which
is considered to have been associated with the adjustment ability of the vasculature itself and the supply of
the offside ICA system through the anterior and posterior communicating arteries.
The research subjects in the present study were all patients with ICA stenosis whose obstruction
occupied more than 80% of the artery. Patients with mild-to-moderate ICA stenosis have a low incidence of
ocular ischemia, the sample size was limited, and it is difficult to detect the hemodynamics of the OA when
it is ischemic. Therefore, a much larger sample with different degrees of ICA stenosis is needed to fully
analyze the hemodynamics of the OA. In addition, we did not investigate the patients’ general condition,
such as the blood pressure, blood glucose level, blood lipid levels, and other risk factors, and no detailed
records were obtained or analysis of the patients’ ocular manifestations was performed in this study. The
main reason for this was that the aim of the study was to complete a preliminary exploration of the feasibility
and value of TCD in detection of changes in the OA blood flow in patients with ICA stenosis. The findings
obtained provide a theoretical and practical basis for subsequent experiments that quantify the hemodynamic
changes of the OA in patients with different degrees of ICA stenosis and other ocular diseases.
In conclusion, TCD allows for an objective evaluation of the hemodynamic changes of the OA in
patients with ICA stenosis, thus clarifying the blood supply of the eye, and has important clinical value in the
diagnosis of ophthalmic diseases. Further study is necessary to explore the correlation between various
changes in the OA blood flow caused by ICA stenosis and other eye diseases.
REFERENCES
1.
2.
3.
4.
5.
Drakou AA, Koutsiaris AG, Tachmitzi SV, Roussas N，Tsironi E， Giannoukas AD et al. The
importance of ophthalmic artery hemodynamics in patients with atheromatous carotid artery disease.
Int Anqiol, 2011, 30(6): 547-554.
Hendrikse J, Klijin CJ, van Huffelen AC, Kappelle LJ , van der Grond J . Diagnosing cerebral
collateral flow patterns: accuracy of non-invasive testing. Cerebrovasc Dis, 2008, 25(5): 430-437.
Chaturvedi S, Bruno A, Feasby T, Holloway R , Benavente O , Cohen SN et al. Carotid
endarterectomy-an evidence-based review: report of the Therapeutics and Technology Assessment
Subcommittee of the American Academy of Neurology. Neurology, 2005, 65(6): 794-801.
Reinhard M, Muller T, Guschlbauer B, Timmer J，Hetzel A. Dynamic cerebral autoregulation and
collateral flow patterns inpatients with severe carotid stenosis or occlusion. Ultrasound in Medicine and
Biology, 2003, 29(8): 1105-1113.
Zhang bin, Ma jingxue, Zhang tongdi，Li tao. The study of hemodynamics in bulbar vessels in patients
of ocular ischemic syndrome. Chin J Pract Ophthalmol, 2006, 24(5): 524-527.
Table 1. Comparison of PSV of the OA between the severe ICA stenosis/occlusion group and the normal
control group
OA
Normal control Positive blood flow in
Reverse blood
group (n = 40)
stenosis/occlusion
flow
in
group (n = 31)
stenosis/occlusion
group (n = 27)
PSV (cm/s)
44.00 ± 2.91
25.10 ± 7.02
52.11 ± 24.30
P value
0.000
0.096
PSV, peak systolic velocity; OA, ophthalmic artery; ICA, internal carotid artery
FIGURES
Figure 1. DSA image of severe stenosis or occlusion in the initial portion of the ICA
Figure 2. Normal blood flow spectrum of the OA
Figure 3. Low-velocity spectrum of the OA
Figure 4. Reverse low-pulsation spectrum of the OA
Figure 5. Reverse high-velocity spectrum of the OA