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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