evaluation of retrobulbar blood flow with color doppler ultrasonography in patients with central...

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Evaluation of Retrobulbar Blood Flow with Color Doppler Ultrasonography in Patients with Central Serous Chorioretinopathy Cihad Hamidi, MD, 1 Fatih Mehmet T urkc u, MD, 2 Cemil Goya, MD, 1 Mehmet G uli C ¸etinc¸akmak,MD, 1 Harun Y uksel, MD, 2 Memik Teke, MD, 1 Salih Hattapo glu, MD, 1 Aslan Bilici, MD 1 1 Department of Radiology, Medical School, Dicle University, Diyarbakir, Turkey 2 Department of Ophthalmology, Medical School, Dicle University, Diyarbakir, Turkey Received 10 July 2013; accepted 13 March 2014 ABSTRACT: Background. To compare retrobulbar blood flow in patients with central serous chorioretin- opathy (CSC) and healthy subjects using color Dopp- ler ultrasonography. Methods. Thirty patients (age 23–54 years) with a first episode of acute CSC and 30 healthy controls (age 30–44 years) were evaluated. The peak systolic blood flow velocity, end-diastolic velocity (EDV), resistance index (RI), and pulsatility index (PI) were measured in the ophthalmic, posterior ciliary, and central retinal arteries. Results. The posterior ciliary and central retinal artery EDV were lower in the patient group than in the control group, whereas RI and PI values were signifi- cantly higher (p < .05). The ophthalmic artery peak systolic blood flow velocity and EDV were lower in the CSC than in the control group (p < .05) without significant difference in RI and PI. Conclusions. Color Doppler ultrasonography pro- vides additional insights into the pathophysiology of CSC and may support the vasospasm hypothesis. V C 2014 Wiley Periodicals, Inc. J Clin Ultrasound 42:481– 485, 2014; Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/jcu.22156 Keywords: central serous chorioretinopathy; color Doppler ultrasonography; resistance index; pulsatility index; central retinal artery C entral serous chorioretinopathy (CSC) is a benign and self-limiting disease, generally observed in young and middle-aged men, and characterized by a serous detachment of the sensorial retina associated with retinal pigment epithelial (RPE) detachment at the macula. 1,2 Type A personality, male gender, emotional dis- tress, pregnancy, hypertension, Cushing’s syn- drome, corticosteroids, and collagen vascular disease are known risk factors for CSC. Although its etiology is still not perfectly known, various factors have been blamed for the condition, 2,3 especially choriocapillary circulatory disorders. Choroidal vasospasm disrupting blood flow would induce lesions of the retinal pigment epithelium, resulting in serous retinal detachment. 4,5 Retrobulbar color Doppler ultrasonography (CDU) is a noninvasive technique that brings useful information about blood flow velocities in the retrobulbar vessels 6 and has been in use for the diagnosis of various ocular diseases since 1989. 7 In this study based on the choriocapillary cir- culation disorder hypothesis, our aim was to compare the retrobulbar blood flow variables, assessed with CDU, in patients with CSC and in healthy subjects. MATERIALS AND METHODS Between December 2011 and June 2012, we eval- uated with CDU 30 patients with a first episode of acute CSC (17 men and 13 women; age 37 6 7.4 years, range 23–54), and 30 healthy con- trol subjects (18 men and 12 women; age 35 6 4.2 years, range 30–44) without any systemic or ocu- lar disease other than refractive errors (from 21 to 1 1 diopter). All patients and healthy controls underwent routine ophthalmologic examination including assessment of visual acuity and direct Correspondence to: C. Hamidi V C 2014 Wiley Periodicals, Inc. VOL. 42, NO. 8, OCTOBER 2014 481

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Page 1: Evaluation of retrobulbar blood flow with color doppler ultrasonography in patients with central serous chorioretinopathy

Evaluation of Retrobulbar Blood Flow withColor Doppler Ultrasonography in Patientswith Central Serous Chorioretinopathy

Cihad Hamidi, MD,1 Fatih Mehmet T€urkc€u, MD,2 Cemil G€oya, MD,1 Mehmet G€uli Cetincakmak, MD,1

Harun Y€uksel, MD,2 Memik Teke, MD,1 Salih Hattapo�glu, MD,1 Aslan Bilici, MD1

1 Department of Radiology, Medical School, Dicle University, Diyarbakir, Turkey2 Department of Ophthalmology, Medical School, Dicle University, Diyarbakir, Turkey

Received 10 July 2013; accepted 13 March 2014

ABSTRACT: Background. To compare retrobulbarblood flow in patients with central serous chorioretin-opathy (CSC) and healthy subjects using color Dopp-ler ultrasonography.

Methods. Thirty patients (age 23–54 years) with afirst episode of acute CSC and 30 healthy controls(age 30–44 years) were evaluated. The peak systolicblood flow velocity, end-diastolic velocity (EDV),resistance index (RI), and pulsatility index (PI) weremeasured in the ophthalmic, posterior ciliary, andcentral retinal arteries.

Results. The posterior ciliary and central retinalartery EDV were lower in the patient group than in thecontrol group, whereas RI and PI values were signifi-cantly higher (p< .05). The ophthalmic artery peaksystolic blood flow velocity and EDV were lower inthe CSC than in the control group (p< .05) withoutsignificant difference in RI and PI.

Conclusions. Color Doppler ultrasonography pro-vides additional insights into the pathophysiology ofCSC and may support the vasospasm hypothesis.VC 2014 Wiley Periodicals, Inc. J Clin Ultrasound 42:481–485, 2014; Published online in Wiley Online Library(wileyonlinelibrary.com). DOI: 10.1002/jcu.22156

Keywords: central serous chorioretinopathy; colorDoppler ultrasonography; resistance index; pulsatilityindex; central retinal artery

Central serous chorioretinopathy (CSC) is abenign and self-limiting disease, generally

observed in young and middle-aged men, andcharacterized by a serous detachment of thesensorial retina associated with retinal pigment

epithelial (RPE) detachment at the macula.1,2

Type A personality, male gender, emotional dis-tress, pregnancy, hypertension, Cushing’s syn-drome, corticosteroids, and collagen vasculardisease are known risk factors for CSC. Althoughits etiology is still not perfectly known, variousfactors have been blamed for the condition,2,3

especially choriocapillary circulatory disorders.Choroidal vasospasm disrupting blood flow wouldinduce lesions of the retinal pigment epithelium,resulting in serous retinal detachment.4,5

Retrobulbar color Doppler ultrasonography(CDU) is a noninvasive technique that bringsuseful information about blood flow velocities inthe retrobulbar vessels6 and has been in use forthe diagnosis of various ocular diseases since1989.7

In this study based on the choriocapillary cir-culation disorder hypothesis, our aim was tocompare the retrobulbar blood flow variables,assessed with CDU, in patients with CSC andin healthy subjects.

MATERIALS AND METHODS

Between December 2011 and June 2012, we eval-uated with CDU 30 patients with a first episodeof acute CSC (17 men and 13 women; age37 6 7.4 years, range 23–54), and 30 healthy con-trol subjects (18 men and 12 women; age 35 6 4.2years, range 30–44) without any systemic or ocu-lar disease other than refractive errors (from 21to 1 1 diopter). All patients and healthy controlsunderwent routine ophthalmologic examinationincluding assessment of visual acuity and direct

Correspondence to: C. Hamidi

VC 2014 Wiley Periodicals, Inc.

VOL. 42, NO. 8, OCTOBER 2014 481

Page 2: Evaluation of retrobulbar blood flow with color doppler ultrasonography in patients with central serous chorioretinopathy

ophthalmoscopy. Diagnosis of CSC was con-firmed by fundus fluorescein angiography andoptical coherence tomography. Acute CSC wasdefined as serous detachment occurring in themacular area and RPE detachment, or dysfunc-tion without evidence of any other possible causeof exudation, such as inflammation, infiltration,or choroidal neovascularization and the durationof any recent subjective symptoms occurringwithin the preceding 3 months.

The exclusion criteria for patients and controlgroup were relapse of acute CSC, chronic CSC,subject smokes, pregnancy, any systemic diseasesuch as hypertension, hyperlipidemia, and dia-betes mellitus, malignancy, coronary artery dis-ease, or history of medical treatment that couldaffect the ocular blood flow within the last 6months (glucocorticoids, statins, b-blockers, psy-chotropic medications, hormonal replacementtherapy).

All patients and controls signed informed con-sent forms before being enrolled in the study.The approval of our institutional review boardwas obtained before the study. All patientsunderwent retrobulbar CDU assessment, per-formed by the same experienced radiologist(C.H.) using an Aplio XG (Toshiba, Tokyo,Japan) device and a 7.5-MHz linear probe. Thepatient was examined in the supine positionwith eyes closed. The ophthalmic, posterior cili-ary, and central retinal arteries were evaluatedand peak systolic blood flow velocity (PSV), end-diastolic velocity (EDV), resistance index (RI),and pulsatility index (PI) were measured.

A sample size of 30 patients per group wasdetermined to be sufficient to detect, with 80%power, a 30% difference between the CSC andthe control groups. The independent samples ttest was used for the statistical analysis carriedout with the Statistical Package for Social Sci-ences software (SPSS 18.0 for Windows; IBM-SPSS, Armonk, NY). A p value< .05 was consid-ered as statistically significant.

RESULTS

Posterior ciliary and central retinal artery EDVwere significantly lower in the patient than inthe control group, whereas RI and PI were sig-nificantly higher (p< .05) (Tables 1 and Table2). There was no significant difference in poste-rior ciliary and central retinal arteries PSVbetween the CSC and the control group. Theophthalmic artery PSV and EDV were signifi-cantly lower in the patient than in the control

group (p< .05). There was no significant differ-ence in ophthalmic artery RI and PI betweenthe two groups (Table 3).

DISCUSSION

Using CDI, our study demonstrated blood flowalterations in CSC patients and supports thehypothesis of choriocapillary circulatory disor-der involvement.

CSC is generally an idiopathic ocular disorderand various factors, such as migraine, depres-sion, type A personality, smoking, stress, preg-nancy, hypertension, treatment with antibiotics,sympathomimetic drugs, systemic corticosteroidtreatment, and vasospasm in the choroidal cir-culation, have been suggested as being involvedin its pathogenesis.2,3,8,9 The diagnosis of CSCis usually made by ophthalmoscopy, with fundusfluorescein angiography and optical coherencetomography as complementary, yet contributive,techniques.10 CDU has been widely used in theevaluation and management of conditions suchas Behcet’s vasculitis, carotid-cavernous fistula,diabetic neuropathy, glaucoma, retinal arteryand vein occlusions, and arteriovenous mal-formations.11–14 CDU allows evaluating the

TABLE 1

Central Retinal Artery Doppler Variables in Patients with

CSC and in Healthy Controls

Doppler Variable CSC Control p

Peak systolic velocity (cm/s) 9.16 9.57 .528

End-diastolic velocity (cm/s) 3.39 4.12 .001

Resistance index 0.61 0.53 .002

Pulsatility index 0.99 0.83 .007

TABLE 2

Posterior Ciliary Arteries Doppler Variables in Patients with

Central Serous CSC and in Healthy Controls

Doppler Variable CSC Control p

Peak systolic velocity (cm/s) 11.3 12.2 .168

End-diastolic velocity (cm/s) 3.59 4.56 .001

Resistance index 0.67 0.6 .003

Pulsatility index 1.16 0.96 <.001

TABLE 3

Ophthalmic Artery Doppler Variables in Patients with CSC

and in Healthy Controls

Doppler Variable CSC Control p

Peak systolic velocity (cm/s) 27.9 33.8 .002

End-diastolic velocity (cm/s) 8.1 10.4 .038

Resistance index 0.69 0.69 .844

Pulsatility index 1.4 1.4 .941

HAMIDI ET AL

482 JOURNAL OF CLINICAL ULTRASOUND

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ophthalmic artery, the posterior ciliary arteries,the central retinal artery, and the central reti-nal vein. The ophthalmic artery is a branch ofthe internal carotid artery and is the mainartery feeding the orbit (Figures 1A and 2A).The central retinal artery and the ciliaryarteries are branches of the ophthalmic artery(Figures 1B and 1C and 2B and 2C).15 The cen-tral retinal artery feeds the retina, while theciliary arteries feed the sclera, choroid, iris, andciliary bodies. CDU is operator-dependent, andreliable Doppler measurements require consid-erable experience by the operator. It is difficultto determine accurately the diameter of orbitalvessels with CDU. Therefore, blood flow velocityas measured with CDU does not necessarilyreflect volumetric blood flow.16

The changes we found in CSC patients sup-port the vasospasm hypothesis.

The posterior ciliary and central retinalartery RI and PI were higher in the patientsthan in the control group, whereas EDV valueswere lower, reflecting increased circulatoryresistance. On the other hand, the ophthalmicartery RI and PI were not significantly differ-ent, because both PSV and EDV were lower in

the CSC than in the control group. As the cen-tral retinal and posterior ciliary arteries supplythe retina and the choroids, increased circula-tory resistance in these vessels in patients withRPE and sensorial retina detachment mayreflect choriocapillary circulatory disorders andsupport the vasospasm hypothesis. Thesearteries receive only a small part of the oph-thalmic artery blood flow, which would not besignificantly altered by these circumscribed cir-culatory changes.

To our knowledge, only one group of investi-gators used Doppler ultrasonography to com-pare retrobulbar blood flow velocities in 16 CSCpatients and in 16 controls.17 Contrary to ourstudy, they found lower RI and PI values in thecentral retinal artery and lower PI values inthe ophthalmic artery in the CSC group. How-ever, their study was performed on a limitednumber of patients. An increase in RI and PI isconsistent with the vasospasm hypothesisbecause vasoconstriction would increase down-stream circulator resistance and compliance.18

Rankin et al. used CDU for the examinationof the central retinal and posterior ciliaryarteries in patients with glaucoma.12 They

FIGURE 1. Images obtained from a 29-year-old man with CSC. (A) Doppler spectra in the ophthalmic artery. (B) Doppler spectra obtained in the

posterior ciliary arteries and (C) central retinal artery.

RETROBULBAR BLOOD FLOW IN CSC

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reported lower posterior ciliary and central reti-nal artery EDV values and higher RI values inthe patients with chronic open-angle glaucomathan in the control group.

Our study has some limitations. The numberof the patients in the control group was small.We did not separately evaluate the short andlong ciliary arteries, which would have beenfeasible with high-frequency imaging usingeither wide-band Doppler or B-flow imaging. Wedid not repeat the Doppler examination aftermedical treatment and during the follow-upperiod, which would be essential for futurestudies.

In conclusion, CDU can demonstratechanges in the retrobulbar blood flow of CSCpatients. Although CDU would have limitedvalue in the diagnosis of CSC, our finding ofincreased vascular resistance in the centralretinal and posterior ciliary arteries maycontribute to a better understanding of itspathogenesis.

REFERENCES

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2. Haimovici R, Koh S, Gagnon DR, et al. Centralserous chorioretinopathy case-control study group.Risk factors for central serous chorioretinopathy: acase-control study. Ophthalmology 2004;111:244.

3. Liew G, Quin G, Gillies M, et al. Central serouschorioretinopathy: a review of epidemiology andpathophysiology. Clin Exp Ophthalmol 2013;41:201.

4. Scheider A, Naseman JE, Lund OE. Fluoresceinand indocyanine green angiographies of centralserous choriodopathy by scanning laser ophthal-moscopy. Am J Ophthalmol 1993;115:50.

5. Kitaya N, Nagaoka T, Hikichi T, et al. Features ofabnormal choroidal circulation in centralserous chorioretinopathy. Br J Ophthalmol 2003;87:709.

6. Baxter GM, Williamson TH. Color Doppler imag-ing of the eye: normal ranges, reproducibility, andobserver variation. J Ultrasound Med 1995;14:91.

FIGURE 2. Images obtained from a healthy 36-year-old man (control group). (A) Doppler spectra in the ophthalmic artery. (B) Doppler spectra

obtained in the posterior ciliary arteries and (C) central retinal artery.

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7. Erickson SJ, Hendrix LE, Massaro BM, et al. ColorDoppler flow imaging of the normal and abnormalorbit. Radiology 1989;173:511.

8. Spahn C, Wiek J, Burger T, et al. Psychosomaticaspects in patients with central serous chorioretin-opathy. Br J Ophthalmol 2003;87:704.

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10. Quin G, Liew G, Ho IV, et al. Diagnosis and inter-ventions for central serous chorioretinopathy:review and update. Clin Exp Ophthalmol 2013;41:187.

11. Ozdemir H, Atilla H, Atilla S, et al. Diagnosis ofocular involvement in Behcet’s disease: value ofspectral and color Doppler sonography. AJR Am JRoentgenol 1995;164:1223.

12. Rankin SJA, Walman BE, Buckley AR, et al. ColorDoppler imaging and spectral analysis of the optic

nerve vasculature in glaucoma. Am J Ophthalmol1995;119:685.

13. Karaali K, Senol U, Aydin H, et al. Optic neuritis:evaluation with orbital Doppler sonography. Radi-ology 2003;226:355.

14. Baydar S, Adapinar B, Kebapci N, et al. ColourDoppler ultrasound evaluation of orbital vessels indiabetic retinopathy. Australas Radiol 2007;51:230.

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16. Stalmans I, Vandewalle E, Anderson DR, et al.Use of colour Doppler imaging in ocular blood flowresearch. Acta Ophthalmol 2011;89:609.

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