Ultrasonic color Doppler imaging to assess the efficacy of orbital decompression in Graves’ ophthalmopathy
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A.A. Kalandari, A.G. Nosova, N.Yu. Kutrovskaya, O.V. Levchenko
Moscow State University of Medicine and Dentistry named after A.I. Evdokimov, Moscow, Russian Federation
Orbital soft tissue ultrasound is particularly important for specialists providing care for Graves’ ophthalmopathy (GO). In addition to echo signs of non-inflammatory edema and/or proliferation of retrobulabar fat, extraocular muscle thickness, their density, and contractility, changes in orbital blood flow should be considered as well. Multiple previous studies demonstrate reduced blood flow in the superior ophthalmic vein. However, recent studies poorly address this issue, therefore, these publications are vital to investigate the problem.
Ultrasonic color Doppler imaging evaluates hemodynamic changes in the orbital blood flow in GO. Changes in linear blood flow velocity in the superior ophthalmic vein are an additional diagnostic criterion for the severity of autoimmune disorder in these patients. Abnormalities of venous blood flow promote non-inflammatory edema of retrobulbar fat, proptosis, and orbital compression. However, linear blood flow velocity in the oph thalmic artery, central retinal artery, and posterior ciliary arteries as well as arterial resistive index should be also considered to predict disease course and to sel ect treatment strategy. Evaluation of hemodynamic changes and their severity can specify the terms and surgical strategy for GO. Being safe and non-invasive tool, ultrasonic colour Doppler imaging can be applied postoperatively. Improved superior ophthalmic vein blood flow fr om orbital soft tissues and reduced resistive index of ophthalmic artery are potential criteria for GO surgery efficacy.
Keywords: Graves’ ophthalmopathy, hemodynamic changes in orbital vessels, superior ophthalmic vein, ophthalmic artery, color-flow duplex scanning, orbital decompression.
For citation: Kalandari A.A., Nosova A.G., Kutrovskaya N.Yu., Levchenko O.V. Ultrasonic color Doppler imaging to assess the efficacy of orbital decompression in Graves’ ophthalmopathy. Russian Journal of Clinical Ophthalmology. 2019;19(3):150–153.
Graves’ ophthalmopathy (GO) is an autoimmune disorder affecting orbital tissues and manifesting by eyelid retraction, edema, exophthalmos, diplopia, and optic neuropathy [1, 2]. Disease severity and activity are similar in patients with unilateral and bilateral orbital lesions as well as in patients with hyper- or hypothyroidism [2, 3]. GO is characterized not only by inflammatory but also hemodynamic changes of orbital tissues which directly or indirectly affect clinical course and manifestations of GO [3-5]. Thus, color Doppler imaging (CDI) demonstrates reduced blood flow in the superior ophthalmic vein [3-7]. CDI while being safe and non-invasive technique to assess regional blood flow evaluates blood flow not only in the superior ophthalmic vein but also in the ophthalmic artery, central retinal artery, central retinal vein, and posterior ciliary arteries .
Despite high efficacy of conservative treatment of GO, many patients require orbital decompression . Just few papers address diagnostic relevance of CDI to assess hemodynamic changes in orbital tissues before and after orbital decompression . These papers describe changes in venous but not arterial blood flow. We have performed complex evaluation of arterial and venous blood flow by CDI in patients with GO before and after orbital decompression.
We have examined 7 women (11 orbits) aged 32-47 years with mild-to-moderate inactive (Clinical Activity Score/CAS < 3) GO. CDI of orbital vessels was performed before and after orbital decompression in July-October 2018. All women were characterized by stable euthyroidism for at least 6 months. All women were diagnosed with mixed GO by preoperative orbit CT scans. Preoperative eye examination included visual acuity and IOP measurements, slit lamp and eye fundus examinations, Hertel exophthalmometry, computer perimetry, and color vision testing. Preoperatively, proptosis was 23-30 mm (on average, 26.5 ± 2.8 mm). In 3 women, exophthalmos was unilateral.
Optic neuropathy, corneal disorders, systemic comorbities (i.e., diabetes, cardiovascular disorders etc.), prior orbital decompression, and smoking were exclusion criteria.
CDI was performed preoperatively, on postoperative day 1 and day 10 and in a month after the surgery using Philips iU22 ultrasound system (12.5 mHz transducer) by a single sonographer. CDI was performed in the supine position with head elevated at 30°. Peak systolic velocity (PSV) and peak diastolic velocity (PDV) were measured, resistivity index (PSV-PDV/PSV) of the ophthalmic artery and central retinal artery were calculated. In addition, maximum and minimum blood flow velocity in the superior ophthalmic vein was measured (see Fig. 1).
External and internal orbital decompression using transcaruncular (via medial wall) or lateral retrocanthal (via lateral wall) approach was performed for cosmetic reasons to regress exophthalmos and upper and lower eyelid herniation. Technical details of the surgery were described previously .
Isolated deep lateral orbitotomy was performed in 8 orbits while deep lateral and medial orbitotomy was performed in 3 orbits. Internal decompression (lipectomy) was performed in all patients. Postoperatively, proptosis was 21-24 mm (on average, 22.5 ± 1.2 mm). Orbital hemodynamic characteristics have significantly improved after orbital decompression (see Table 1).
Multiple studies demonstrate reduced blood flow in the superior ophthalmic vein in patients with GO [3-7]. Recent studies on this issue are scarce, therefore, these papers are essential. Our findings demonstrate that despite the differences between maximum and minimum blood flow velocity in the superior ophthalmic vein, these parameters tend to increase after orbital decompression. This phenomenon confirms that external compression of blood vessels by hypertrophic soft tissues (i.e., orbital fat or extraocular muscles) is the leading cause of hemodynamic abnormalities in GO. Other potential factors of impaired venous drainage (i.e., systemic high blood pressure or elevated intraocular pressure) are insignificant [1, 11].
Obviously, impaired venous drainage resulting from external compression aggravates exophthalmos, chemosis, and eyelid edema in GO. External compression can result in reduced blood flow but also in superior ophthalmic vein thrombosis (see Fig. 2). Some authors suggest that this is venous stasis (one of the elements of Virchow’s triad) that predisposes to the thrombosis . Superior ophthalmic vein thrombosis is a rare condition which can result in vision loss due to the compartment syndrome or secondary glaucoma [12, 13].
Our preliminary results demonstrate that orbital decompression to increase orbital volume and to reduce orbital congestion elevates blood flow velocity in the superior ophthalmic vein and ophthalmic artery. М. Pérez-López et al. have also demonstrated significant decrease in RI of the superior ophthalmic vein and ophthalmic artery after decompression orbitotomy .
There are two hypotheses on high preoperative RIs of the superior ophthalmic vein and ophthalmic artery . The first hypothesis is based on the external compression of orbital vessels by abnormal extraocular muscles or hypertrophic orbital fat resulting from prior inflammation. The second hypothesis directly correlates with the nature and severity of inflammatory changes of the orbital contents at the time of disease manifestation or activation .
Our findings and М. Pérez-López et al. study  confirm the first hypothesis since all patients were characterized by stable euthyroidism and CAS less than 3.
Our study has some limitations, in particular, small sample size and the lack of the control group. However, preliminary results demonstrate the advantages of CDI as the method of efficacy control of orbital decompression in GO. Considering informative value and safety of this technique, preoperative CDI data can be used as one of the criteria of surgical indications for GO in addition to other clinical, laboratory, and instrumental tests. Evaluation of orbital hemodynamics in optic neuropathy before and after the surgery is of particular importance. The effect of various types of orbital decompression on venous and arterial blood circulation in GO still remains elusive. Further randomized studies are required.
CDI is an informative non-invasive ultrasound technique to assess orbital vessels both in GO and complications of this autoimmune disorder (e.g., optic neuropathy). Being safe and non-invasive tool, CDI can be applied preoperatively to determine surgical indications. Reduced linear blood flow in the superior ophthalmic vein and increased RI of the ophthalmic artery may contribute to the selection of orbital decompression technique for GO. Improved blood flow in the superior ophthalmic vein and reduced RI of the ophthalmic artery revealed by CDI are potential criteria for the efficacy of GO surgery.
About the authors:
Alik A. Kalandari — MD, PhD, neurosurgeon, Deputy Medical Director of CMC, ORCID iD 0000-0003-4161-0940;
Anastasiya G. Nosova — MD, specialist in ultrasound examination of CMC, ORCID iD 0000-0003-3066-0117;
Natal’ya Yu. Kutrovskaya — MD, PhD, neuro-ophthalmologist of CMC, ORCID iD 0000-0002-3202-570X;
Oleg V. Levchenko — MD, PhD, Medical Prorector, ORCID iD 0000-0003-0857-9398.
Moscow State University of Medicine and Dentistry named after A.I. Evdokimov. 20/1, Delegatskaya str., Moscow, 127473, Russian Federation.
Contact information: Alik A. Kalandari, e-mail: email@example.com. Financial Disclosure: no author has a financial or property interest in any material or method mentioned. There is no conflict of interests. Received 08.11.2018.
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