Russian Journal of Clinical Ophthalmology
ISSN 2311-7729 (Print), 2619-1571 (Online)

Ophthalmological monitoring in patients with hypertension and coronary heart disease

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DOI: 10.32364/2311-7729-2021-21-2-51-57

L.K. Moshetova1, I.V. Vorobyeva1, A. Dgebuadze1, O.D. Ostroumova1,2, A.V. Arablinskiy1,2, E.P. Delver3, A.A. Belogurov3

1Russian Medical Academy of Continuous Professional Education, Moscow,
 Russian Federation

2S.P. Botkin City Clinical Hospital, 5, 2nd Botkinskiy passage, Moscow, Russian Federation

3National Medical Research Center of Cardiology, Moscow, Russian Federation

Aim: to study ophthalmological clinical functional parameters in patients with hypertension and coronary heart disease (CHD) with coronary artery stenosis.

Patients and Methods: 30 patients (58 eyes) with hypertension and CHD with coronary artery stenosis (group A) and 30 healthy controls (60 eyes, group B) were examined. Best-corrected visual acuity (BCVA), macular sensitivity (MS) assessed by MAIA microperimetry, central macular thickness (CMT), foveal avascular zone (FAZ) area, vessel density of superficial capillary plexus (SCP VD) and deep capillary plexus (DCP VD) and choriocapillaris measured by optical coherence tomography angiography (OCTA) were evaluated.

Results: FAZ area was 0.42±0.03 mm2 in group A and 0.28±0.03 mm2 in group B (p<0.05). SCP VD was 11.4±3.1% in group A and 25.4±2.5% in group B (p<0.05). DCP VD was 22.3±1.1% in group A and 39.2±3.5% in group B (p<0.05). Choriocapillaris VD was 51.2±1.1% in group A and 63.1±1.2% in group B (p<0.05). Correlations between ocular parameters and ejection fraction (EF) were revealed (BCVA: r=0.61, p<0.05; MS: r=0.68, p<0.05; CMT: r=-0.72, p<0.05; FAZ: r=-0.73, p<0.05; SCP VD: r=0.82, p<0.05; DCP VD: r=0.81, p<0.05; choriocapillaris VD: r=0.76, p<0.05).

Conclusions: in patients with hypertension and CHD with coronary artery stenosis, significant (p<0.05) reduction in BCVA, MS, SCP VD, DCP VD, and choriocapillaris VD and increase in CMT and FAZ area were detected compared to healthy individuals. Additionally, strong correlations between ocular parameters (FAZ, SCP VD, DCP VD, and choriocapillaris VD) and EF (p<0.05) were identified. OCTA may be recommended to monitor fundus vessels in hypertension and CHD as an effective noninvasive valuable diagnostic tool to verify hypertension and CHD.

Keywords: hypertension, coronary heart disease, coronary artery stenosis, hypertensive retinopathy, foveal avascular zone, vessel density, optical coherence tomography angiography.

For citation: Moshetova L.K., Vorobyeva I.V., Dgebuadze A. et al. Ophthalmological monitoring in patients with hypertension and coronary heart disease. Russian Journal of Clinical Ophthalmology. 2021;21(2):51–57. DOI: 10.32364/2311-7729-2021-21-2-51-57.

Background

Essential hypertension (EH) and coronary heart disease (CHD) are the leading causes of death worldwide [1, 2]. The major complication of hypertension is microvascular damage resulting from impaired vasomotor tonus and increased vascular resistance due to high blood pressure (BP) [3]. The key triggers of CHD are atherosclerosis, vascular spasm, and progressive chronic inflammation associated with thickening or stenosis of vascular wall. Previously, numerous studies on the association between EH and retinal circulation were conducted. Hypertensive ocular funduscopic abnormalities include classic signs of hypertensive retinopathy, e.g., arteriovenous crossings, generalized or focal narrowing of arterioles, microaneurisms, intraretinal hemorrhages, cotton-wool spots, and optic disc edema. These abnormalities increase the risk of systemic disorders, i.e., stroke and cardiovascular diseases [6, 7]. Larger retinal vessels (200–300 μm) were also evaluated on color fundus images. The correlation between the diameter of arterioles and EH stage was established [3]. Risk factors of CHD are described in detail and well-known. However, methods and markers to stratify patients by the risk of CHD are still of interest.

There are two sources of retinal blood supply, i.e., retinal vessels and choriocapillaris. Retinal blood vessels supply five inner retinal layers. Five outer retinal layers are almost avascular and receive oxygen and nutrients from choriocapillaris. Both retinal and choroidal blood vessels are supplied from the ophthalmic artery (a terminal branch of the coronary artery). Since retinal vessels are about the same size as the coronary microcirculation (~100–250 μm), they may be representative of the processes occurring in subclinical coronary stenosis [8].

Retinal vascular abnormalities are detected by fundus biomicroscopy, fundus photography, and fluorescein angiography (FA). Despite the invasiveness of FA (IV injection of a contrast agent) and side effects of fluorescein, FA is considered the gold standard for vascular imaging for more than 50 years [9]. Recently, optical coherence tomography angiography (OCTA), a novel noninvasive technique of fundus vascular imaging, was introduced into clinical practice. OCTA is a useful tool for the early diagnosis of many ocular disorders, i.e., age-related macular degeneration (AMD) [10], diabetic retinopathy (DR) [9], and hypertensive retinopathy [11].

Prior studies have demonstrated the association between retinal microvascular abnormalities and CHD. Thus, Tabatabaee et al. (2013) revealed a strong correlation between atherosclerosis of retinal arteries and CHD severity [12]. Wong et al. revealed correlations between narrowing of retinal arterioles and CHD development by measuring the diameter of individual arterioles and venules on fundus photos [13]. However, we failed to find any studies on the association between EH, CHD, and retinal/choroidal vascular abnormalities using OCTA.

Scientists worldwide currently study retinal blood flow and vessel density by OCTA that evaluates vessel density in various anatomical layers of eye fundus [14, 15]. OCTA allows for evaluating foveal avascular zone (FAZ) area, vessel density of superficial capillary plexus (SCP VD), deep capillary plexus (DCP VD), and choriocapillaris (CC VD). Meanwhile, studies on retinal vessel density in EH produce controversial findings, i.e., increased/reduced FAZ, SCP VD, DCP VD, and CC VD [3, 11, 16–21]. Considering these controversial findings, we undertook this research.

Aim

To study ophthalmological clinical functional parameters in patients with EH and CHD and coronary artery stenosis. 

Patients and Methods 

Sixty patients (118 eyes) were examined. Group A included 30 patients (58 eyes) with EH (stage 1, 2, or 3) and CHD (stable angina). Group B included 30 healthy controls (60 eyes) without EH or CHD. The mean age was 64.7 ± 0.95 years. Group A patients regularly seen a cardiologist and received medical therapy (according to the guidelines of the Russian Society of Cardiology). CHD and coronary artery stenosis were verified by coronary angiography. The duration of EH and CHD was less than 5 years in 15 patients (50%), 6 to 10 years in 10 patients (33.3%), 11 to 15 years in 3 patients (10%), and more than 15 years in 2 patients (6.6%). During the follow-up, BP was stabilized (135/85 mm Hg) in 30 group A patients. Eye fundus abnormalities were classified using the M.L. Krasnov grading system for hypertensive retinopathy (1948) that includes four stages, i.e., hypertensive angiopathy, hypertensive angiosclerosis, hypertensive retinopathy, and hypertensive neuroretinopathy.

To identify retinal microvascular abnormalities, macular sensitivity (MS), central macular thickness (CMT), FAZ area, SCP VD, DCP VD, and CC VD measured by OCTA were compared between patients with EH and CHD with coronary artery stenosis and healthy controls.

All participants underwent a complex eye examination, which included best-corrected visual acuity (BCVA) and intraocular pressure (IOP) measurements, slit lamp examination, fundus biomicroscopy, MAIA microperimetry (CenterVue Spa, Italy), and OCTA (Optovue, USA). Coronary angiography was performed using Allura Xper FD20 (Philips Medical Systems Nederland B.V., the Netherlands).

Inclusion criteria in group A were compensated EH and stable angina (angina pectoris) and coronary artery stenosis. Exclusion criteria were severe somatic comorbidities (e.g., liver or kidney diseases, cardiovascular or nervous system disorders), diabetes, secondary hypertension, acute myocardial infarction, stroke, other cardiovascular and blood disorders of any origin. Inclusion criteria in group B were the lack of any cardiovascular or systemic diseases affecting blood vessels of eye fundus.

Ophthalmological exclusion criteria in group A and B were inflammatory ocular diseases, glaucoma, moderate to high refractive errors, (im)mature cataract, and significant opacities of the optical media that potentially affecting OCTA imaging.

OCTA

Before OCTA, dilating eye drops (tropicamide 0.8% + phenylephrine 5.0%) were instilled three times within 15 min. Additionally, anesthetic eye drops (proxymetacaine hydrochloride 0.5%) were instilled to minimize blinking. After pupil dilation, OCTA was performed twice with a 5-min interval in the same position to obtain images of the macular microvasculature (3×3 mm). 3×3 mm scan area was divided into five subfields composed of a 1-mm center and four quadrants (superior, inferior, inner, and outer). The device automatically measured FAZ area at every scanning and performed a segmentation by the following borders: superficial capillary plexus (see Fig. 1A) with the inner border 3 µm below the internal limiting membrane and the outer border 15 µm below the inner plexiform layer; deep capillary plexus (see Fig. 1B) with the inner border 15 µm below the inner plexiform layer and the outer border 70 µm below the inner plexiform layer; choriocapillaris (see Fig. 1C), 30 µm to 60 µm below the level of the retinal pigment epithelium (RPE).
 

Рис. 1. Оптическая когерентная томография с ангиографией: А — поверхностное сосудистое сплетение, В — глубокое сосудистое сплетение, С — слой хориокапилляров Fig. 1. Optical coherence tomography angiography: A — superficial vascular plexus, B — deep vascu

Results 

In group A (58 eyes), hypertensive angiopathy was diagnosed in 25 eyes (43.1%), hypertensive angiosclerosis in 26 eyes (44.8%), hypertensive retinopathy in 6 eyes (10.3%), and hypertensive neuroretinopathy in 1 eye (1.7%). The principal ophthalmological parameters in groups A and B are listed in Table 1.

Таблица 1. Основные офтальмологические показатели в группах А и B Table 1. Key functional parameters in groups A and B


Fig. 2 illustrates the data of a 65-year-old man who was diagnosed with EH stage 3, high (stage 4) risk of cardiovascular complications, CHD (stable angina, NYHA class II), and hypertensive angiopathy. The BCVA of the right eye was 20/25. MAIA microperimetry revealed a reduction in MS to 12.6 dB without any significant abnormalities on fundus photos and horizontal OCT scans.

Рис. 2. Клиническое наблюдение: пациент Ф., 65 лет, правый глаз: А — фото глазного дна, В — фундус-микропериметрия MAIA, С — горизонтальный ОКТ-скан макуляр- ной зоны Fig. 2. Right eye of a 65-year-old man: A — fundus photo, B — MAIA microperimetry, C — h

The measurement of FAZ area was of particular importance. In group B, FAZ area was 0.28 ± 0.03 mm2. In group A, FAZ area was significantly higher (0.42 ± 0.03 mm2, p < 0.05).

Vessel density measured by OCTA is the strongest indicator of the impairment of fundus microcirculation (see Fig. 3).

Рис. 3. Плотность сосудов поверхностного (А) и глубокого (В) сплетений сетчатки и в слое хориокапилляров (С) у пациентов исследуемых групп Fig. 3. SCP VD (A), DCP VD (B), and choriocapillaris VD (C) in patients with hypertension and CHD and healthy contro

OCTA has demonstrated that SCP VD was lower in group A compared to group B in all areas investigated, i.e., 11.4 ± 3.1% vs. 25.4 ± 2.5% (p < 0.05) in the fovea, 40.4 ± 4.1% vs. 50.5 ± 2.5% (p < 0.05) in the superior sector, 41.3 ± 2.5% vs. 48.8 ± 3.1% (p < 0.05) in the nasal sector, 44.3 ± 2.4% vs. 50.6 ± 3.1% (p < 0.05) in the inferior sector, and 42.6 ± 2.4% vs. 50.3 ± 3.7% (p < 0.05) in the temporal sector.

Fig. 4A illustrates coronarography of a 66-year-old man diagnosed with EH and CHD that revealed the stenosis of the anterior descending artery (>70%). OCTA (see Fig. 4B) identified reduced retinal SCP VD in most investigated areas, i.e., by 17% in the fovea, 43% in the nasal sector, 44% in the inferior sector, and 45% in the temporal sector. Fig. 4C illustrates SCP VD map of a healthy individual without EH or CHD (VD in the fovea is 31% and VD in parafovea is 54–58%).

Рис. 4. Клиническое наблюдение: данные коронарографии (А) и карта плотности сосудов поверхностного сплетения сетчатки (В) пациента Б., 66 лет, с ГБ и ИБС, в сравнении с данными карты плотности сосудов поверхностного сплетения сетчатки (С) у здорового чело

A significantly greater reduction in DCP VD and CC VD was revealed in patients with EH and CHD (p < 0.01). In group A and B, DCP VD was 22.3 ± 1.1% and 39.2 ± 3.5% (p < 0.05) in the fovea, 49.1 ± 3.7% and 64.3 ± 4.3% (p < 0.05) in the superior sector, 50.2 ± 3.1% and 64.2 ± 4.1% (p < 0.05) in the nasal sector, 52.2 ± 3.6% and 65.1 ± 3.7% (p < 0.05) in the inferior sector, and 52.7 ± 3.1% and 61.1 ± 3.9% (p < 0.05) in the temporal sector, respectively.

In group A and B, CC VD was 51.2 ± 1.1% and 3.1 ± 1.2% (p < 0.05) in the fovea, 48.1 ± 2.2% and 65.2 ± 1.2% (p < 0.05) in the superior sector, 49.3 ± 1.2% and 66.8 ± 1.2% (p < 0.05) in the nasal sector, 49.1 ± 1.2% and 66.2 ± 1.1% (p < 0.05) in the inferior sector, and 50.7 ± 1.1% and 65.2 ± 1.6% (p < 0.05) in the temporal sector, respectively.

Significant correlations between ejection fraction (EF) measured by echocardiography and ocular parameters were revealed in patients with EH and CHD (see Fig. 5), i.e., r = 0.61 for BCVA (p < 0.05), r = 0.68 for MS (p < 0.05), r = -0.72 for CMT (p < 0.05), r = -0.73 for FAZ (p < 0.05), r = 0.82 for SCP VD (p < 0.05), r = 0.81 for DCP VD (p < 0.05), and r = 0.76 for CC VD (p < 0.05).

Рис. 5. Корреляционные взаимосвязи фракции выброса левого желудочка с офтальмологическими показателями (МКОЗ, СМ, ЦТС, ФАЗ, ПСПС, ПСГС, ПСХ) Fig. 5. Correlations between left ventricular ejection fraction and ocular parameters (BCVA, MS, CMT, FAZ, SCP VD,

Discussion

Currently, scientists worldwide extensively study the associations between retinal vessel density and CHD. The severity of retinal artery atherosclerosis correlates with the severity of CHD. The association between the narrowing of retinal arterioles and the development of EH and CHD was also established. Meanwhile, the diameter of retinal vessels, in particular, arterioles, allows for predicting the risk of EH and CHD. However, all these studies were conducted in patients with EH and CHD with clinically apparent vascular abnormalities of eye fundus [8].

In addition to ophthalmoscopic abnormalities, we evaluated MS, SCP VD, DCP VD, and CC VD in patients with EH and CHD and coronary artery stenosis, even in the lack of clinically apparent fundus abnormalities. Abnormalities diagnosed by OCTA with the assessment of vessel density may be representative of the severity of cardiovascular disorders. Thus, noninvasive OCTA is characterized by a higher resolution compared to classic FA and indocyanine green angiography (ICG) [22]. OCTA allows precise localization of pathological process in both retinal and choroidal microcirculation. Meanwhile, FA is used for observing retinal vessels and ICG is more suitable for visualizing choroid [23]. Coronary angiography is the gold standard to diagnose cardiovascular diseases [24].

We have demonstrated a significant reduction in vessel density in most retinal sectors in group A compared to group b (p < 0.05). Additionally, a significant decrease in BCVA was revealed in group A. MAIA microperimetry detected a reduction in retinal sensitivity before morphological abnormalities identified by OCT occurred. CMT was significantly higher in patients with EH and CHD with coronary artery stenosis compared to healthy individuals.

In EH and CHD, modern diagnostic tools (OCTA and MAIA microperimetry) revealed a significant reduction in SCP VD, DCP VD, and CC VD before fundus abnormalities appeared. Therefore, OCTA is an effective noninvasive technique to detect fundus vascular abnormalities in EH and CHD. Ophthalmic monitoring of patients with EH and CHD effectively reduces the risk of ocular complications.

Conclusions

1. In patients with EH and CHD with coronary artery stenosis, significant reduction in BCVA (p < 0.05), MS (p < 0.05), SCP VD (p < 0.05), DCP VD (p < 0.05), and CC VD (p < 0.05) and increase in CMT (p < 0.05) and FAZ area (p < 0.05) was detected compared to healthy individuals.

2. In patients with EH and CHD with coronary artery stenosis, correlations between ophthalmic parameters and EF were also identified, i.e., FAZ (r = -0.73, p < 0.05), SCP VD (r = 0.82, p < 0.05), DCP VD (r = 0.81, p < 0.05), and CC VD (r = 0.76, p < 0.05).


About the authors:

1Larisa K. Moshetova — Doct. of Sci. (Med.), Professor, Full- Member of the Russian Academy of Sciences, Honored Doctor of Russian Federation, President of the Russian Medical Academy of Continuous Professional Education, Head of the Department of Ophthalmology, ORCID iD 0000-0002-5899-2714;

1Irina V. Vorobyeva — Doct. of Sci. (Med.), Associate Professor of the Department of Ophthalmology, ORCID iD 0000-0003-2707-8417;

1Ana Dgebuadze — postgraduate student of the Department of Ophthalmology, ORCID iD 0000-0002-9518-0459;

1,2Olga D. Ostroumova — Doct. of Sci. (Med.), Professor, Head of the Department of Therapy & Polymorbid Diseases, ORCID iD 0000-0002-0795-8225;

1,2Aleksandr V. Arablinskiy — Doct. of Sci. (Med.), Professor of the Department of Therapy & Polymorbid Diseases, ORCID iD 0000-0002-2117-5016;

3Evgeniy P. Delver — Doct. of Sci. (Biol.), Senior Researcher, ORCID iD 0000-0003-2319-7937;

3Anatoliy A. Belogurov — Doct. of Sci. (Biol.), Leading Researcher, ORCID iD 0000-0003-1594-9035.

1Russian Medical Academy of Continuous Professional Education. 2/1, Barrikadnaya str., Moscow, 123995, Russian Federation.

2S.P. Botkin City Clinical Hospital. 5, 2nd Botkinskiy passage, Moscow, 125284, Russian Federation.

3National Medical Research Center of Cardiology. 15A, 3rd Cherepkovskaya str., Moscow, 121552, Russian Federation.


Contact information: Ana Dgebuadze, e-mail: dgebuadzeana@yahoo.com. Financial Disclosure: no authors have a financial or property interest in any material or method mentioned. There is no conflict of interests. Received 15.03.2021. 



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