Abstract
The retina is supplied by two circulations: the choroidal circulation via the choroidal vessels and the retinal circulation via the central retinal artery (Jakobiec 1982). In up to 32% of the eyes (Justice and Lehmann 1976), an additional branch, the cilioretinal artery, may extend from the choroidal circulation to supply a portion of the inner retina, mainly in the macular region.
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Anatomy of the Retinal Vascular System
The retina is supplied by two circulations: the choroidal circulation via the choroidal vessels and the retinal circulation via the central retinal artery (Jakobiec 1982). In up to 32% of the eyes (Justice and Lehmann 1976), an additional branch, the cilioretinal artery, may extend from the choroidal circulation to supply a portion of the inner retina, mainly in the macular region.
The choroidal circulation is supplied by the ophthalmic artery via the medial and lateral posterior ciliary arteries, each of which gives rise to one long and multiple short posterior ciliary arteries. Apart from minor contributions from recurrent branches of the long posterior ciliary arteries, the choriocapillaris is supplied by the short posterior arteries, which penetrate the posterior globe near the optic nerve (Oyster 1999). Paula et al. demonstrated that there is a higher arteriolar supply from the posterior ciliary artery surrounding the macula than the rest of the retina, with approximately nine pairs of arterioles and venules distributed in the parafoveal regions (Paula et al. 2010).
It was previously thought that branches from the central retinal vessels form only two distinct capillary beds, one in the nerve fiber layer (superficial capillary plexus or SCP) and the other in the deep boundary between the inner nuclear layer and the outer plexiform player (deep capillary plexus or DCP) (Grant and Lutty 2012). Until recently, the visualization of these capillary systems remained inaccessible except via fluorescein angiography (FA). Weinhaus et al. reported that the SCP was visualized over four times more effectively than the DCP in FA, thereby limiting the understanding of the vascular pathology affecting these deeper layers (Weinhaus et al. 1995).
The development of optical coherence tomography angiography (OCTA) allowed visualization of the deeper capillaries with sufficient detail to evaluate the impact of various vascular disorders at this level. Park et al. utilized OCTA to distinguish a middle capillary plexus (MCP) from the SCP and DCP which lies at the inner boundary of the inner nuclear layer (Park et al. 2016) (Fig. 11.1). Around the optic nerve, an additional fourth, more superficial capillary network, the radial peripapillary capillaries, exists (Max Snodderly and Weinhaus 1990).
Fluorescein Angiography and Wide-Angle Imaging in Retinal Vascular Disease
Diabetic Retinopathy
Retinal capillary microaneurysms develop as a saccular outpouching from the capillary wall (Akram et al. 2013) and are readily detected in the early frames of FA where they appear as small hyperfluorescent dots. They may also show variable leakage which fades in the later frames. FA helps distinguish them from clinically similar tiny punctate dot hemorrhages that will generally block fluorescence (de Venecia et al. 1976) (Fig. 11.2).
Intraretinal microvascular abnormalities (IRMA) is a term used to describe clusters of abnormal hypercellular vascular structures that arise on the edges of areas of retinal capillary non-perfusion (Davis et al. 1968). Clinically, it can be difficult to distinguish IRMA from neovascularization (NV). On FA, IRMAs typically do not show leakage whereas NV does (Fig. 11.3).
In DR, distortion and enlargement of the foveal avascular zone (FAZ) result from occlusion of retinal capillaries and loss of precapillary arterioles near the fovea (Fig. 11.4). This was extensively documented by Conrath et al. (2005), Arend et al. (1995) and Bresnick et al. (1984). However, areas of non-perfusion may be underappreciated on FA because of the diffuse leakage from surrounding vessels, especially in later frames.
Proliferative diabetic retinopathy (PDR) is characterized by the development of neovascularization at or around the disc (NVD) or surrounding areas of ischemia in the periphery, referred to as neovascularization elsewhere (NVE). NVD and NVE appear hyperfluorescent and tend to exhibit leakage on FA and wide field imaging (Figs. 11.5 and 11.6).
Diabetic macular edema (DME) is characterized by macular thickening caused by leakage from hyperpermeable vasculature (Wilkinson et al. 2003). It can be appreciated by FA as leaking of the dye in early frames, typically in a petalloid or honeycomb pattern (Otani and Kishi 2007) (Fig. 11.7). Borders of edematous retinal tissue may show waxy yellowish deposits, known as hard exudates. They form as a result of leakage of lipoprotein and fluid from damaged capillaries into the extracellular space of the retina (Ferris and Patz 1984). Increased amounts of hard exudate within the 30° photographic field centered on the macula has been associated with a higher risk of visual impairment (Chew et al. 1996).
Retinal Vein Occlusion
The clinical presentation of retinal vein occlusion (RVO) may vary according to the site of the occlusion. A branch occlusion (BRVO) typically occurs at the site of an arterio-venous crossing, while central retinal vein occlusions (CRVO) occur at the level of the lamina cribrosa (Browning 2012).
Fundus photographs reveal extensive intraretinal hemorrhage and exudation in the area drained by the occluded vein which appears tortuous and dilated. The optic nerve head may also appear elevated, hyperemic and swollen, particularly in central vein involvement. Long standing cases may be associated with the development of optociliary collaterals, NV and the development of fibrous tissue (Hayreh et al. 1983; Murakami et al. 1983). On FA, acutely there is typically a delay in arteriovenous transit followed by staining of the walls of the affected veins. This is accompanied by capillary non-perfusion and extensive leakage distal to the site of the occlusion (Clemett 1974) (Figs. 11.8 and 11.9). In cases where the macular circulation is involved, extensive leakage of the fluorescein dye is seen in or around the fovea. In long standing ischemic cases, FA may demonstrate the development of NVD or NVE, which appear as hyperfluorescent leaking areas in the later frames (Hayreh et al. 1983).
Retinal Artery Occlusion
Occlusion of the retinal arterial supply may occur at different levels, including the main trunk of the central retinal artery (CRAO), one of the terminal branches of the central artery (BRAO) or, in some cases, the cilioretinal branch of the short posterior ciliary arteries. Clinically, the diagnosis of retinal artery occlusion has commonly been based on clinical findings of retinal thickening and whitening in the area supplied by the occluded vessel. In case of CRAO, a cherry red spot can be appreciated at the site of the fovea. In acute presentations, FA reveals a delay in retinal arterial filling, as well as arteriovenous transit time. FA also shows hypofluorescence of the affected area caused by thickening and swelling of the tissue and “cattle-trucking” of the blood column in the branch arteries (Beatty and Eong 2000) (Fig. 11.10).
Sickle Cell Retinopathy
Sickle cell retinopathy is characterized by an initial non-proliferative phase characterized by vascular tortuousity, salmon patch hemorrhages between the internal limiting membrane (ILM) and the retinal surface, intraretinal hemorrhages and dark areas of RPE hyperpigmentation known as black sunbursts. Eventually, prolonged retinal ischemia and peripheral capillary non-perfusion results in the development of the proliferative phase, characterized by NV, which acquires a “sea fan” configuration, subhyaloid and/or vitreous hemorrhage as well as tractional or combined tractional-rhegmatogenous retinal detachment (Goldberg 1971).
FA remains the most widely used tool in the assessment of patients with sickle cell retinopathy to evaluate peripheral capillary non-perfusion, particularly temporally, as well as hyperfluorescent leaking NV in the earlier frames of the angiogram (Rednam et al. 1982). Owing to the peripheral nature of the retinal pathology, wide-field FA is of particular importance in these cases where some areas, particularly those close to the ora serrata, may be missed by conventional FA (Cho and Kiss 2011) (Fig. 11.11). FA may also demonstrate an enlarged FAZ. Clinically, the optic disc may exhibit small dilated capillaries that are occluded on FA (Goldbaum et al. 1978; Condon and Serjeant 1972; Moriarty et al. 1988). Later stages of sickle cell retinopathy with development of fibroglial tissue may show staining of these membranes in the later frames of the angiogram.
Optical Coherence Tomography in Retinal Vascular Disease
Diabetic Macular Edema
Clinically significant macular edema (CSME) is defined as the clinical detection of any one of the following: thickening of the retina located 500 μm or less from the center of the macula, hard exudates with thickening of the adjacent retina 500 μm or less from the center of the macula, or a zone of retinal thickening one disc area or larger in size, located 1 disc diameter (DD) or less from the center of the macula. OCT DME is defined as thickening of the retina with or without partial loss of transparency within 1 DD from the center of the macula (Klein et al. 1995). OCT may also reveal distortion of the structural retinal anatomy caused by the accumulation of intraretinal and subretinal fluid (Hee et al. 1995) (Fig. 11.12).
OCT also provides a quantitative retinal thickness map, thus allowing easier and more thorough follow-up (Fig. 11.13). On the other hand, it is worth noting that there is no direct correlation between retinal thickness and visual acuity. Patients with higher retinal thickness may show paradoxical better visual acuity than those with lower retinal thickness, and vice versa (Network 2007) (Fig. 11.14).
Using SD-OCT, Sun et al. found a correlation between the detection of disorganization of the retinal inner layers (DRIL) in patients with DME and worsening of visual acuity (Sun et al. 2014). It may be attributed to the higher incidence of DCP affection and photoreceptor involvement associated with DRIL (Onishi et al. 2019) (Fig. 11.15).
Retinal Vein Occlusion
SD-OCT is a helpful tool in the assessment of the macular involvement in cases of RVO. Macular edema is typically characterized by marked thickening and/or interruption of the retinal layers accompanied by the development of hypo-translucent cystic spaces (Hee et al. 1995). Long-standing cases show higher incidences of development of epiretinal membranes, which are can be readily monitored by OCT (Mitchell et al. 1997) (Fig. 11.16).
Retinal Artery Occlusion
SD-OCT has been used in retinal artery occlusion to visualize the effect of non-perfusion on the structural integrity of the retinal layers. Increased reflectivity and thickness of the inner retina in early presentations as a result of swelling and thickening has been documented on OCT. These findings are followed by a decrease in reflectivity and thickness of the inner retina, as well as an increase in reflectivity in the outer retina and RPE/choriocapillaris layer attributed to atrophy of the neurosensory retina (Ahn et al. 2015; Falkenberry et al. 2006; Yu et al. 2015).
Acute Macular Neuroretinopathy and Paracentral Acute Middle Maculopathy
SD-OCT, as well as OCTA, have allowed better characterization of distinct manifestations of retinal ischemia named acute macular neuroretinopathy (AMN) and paracentral acute middle maculopathy (PAMM).
Clinically, AMN is characterized by the presence of intraretinal, reddish-brown, wedge-shaped lesions, commonly in the perifoveal area. A characteristic feature of these wedges is that their apices tend to point to the fovea (Bos and Deutman 1975; Bhavsar et al. 2016). They are commonly unimpressive on fundus photographs and are better appreciated on infrared imaging as parafoveal hyporeflective lesions.
FA does not add to the clinical findings and does not greatly help in the diagnosis of AMN (Priluck et al. 1978). During the acute phase of the lesion, SD-OCT shows a transient hyperreflectivity of the OPL and ONL. Within days, this hyperreflectivity begins to resolve and is followed by an interruption of the interdigitation zone (RPE/outer segment junction) and the ellipsoid zone (inner segment/outer segment junction or IS/OS), as well as thinning of the outer nuclear layer (ONL). Over time, symptoms may improve despite the persistence of some OCT findings including ONL thinning and interruption of the interdigitation zone (Fawzi et al. 2012) (Fig. 11.17).
PAMM was introduced by Sarraf et al. while documenting lesions similar to AMN but involving the middle macular region above the outer plexiform layer (Sarraf et al. 2013). Sridhar et al. described three distinct en face OCT patterns in PAMM: arteriolar, fern-like, and globular (Sridhar et al. 2015). As with AMN, PAMM lesions may pass into thinning of the affected layers, primarily the inner nuclear layer (INL) (Rahimy et al. 2015) (Fig. 11.18).
As a result, SD-OCT and OCTA, in addition to near-infrared reflectance and red-free imaging, are the current imaging modalities for the detection of the subtle retinal changes associated with PAMM and AMN.
Sickle Cell Retinopathy
SD-OCT is helpful in demonstrating the consequences of sickle ischemic maculopathy, even in cases that are undetectable on FA. Murthy et al. found atrophy of the inner retinal layers of patients with sickle cell retinopathy (Murthy et al. 2011). This finding was also corroborated by Witkin et al. and was attributed to the occurrence of a macular infarction as a result of an ischemic vaso-occlusive episode (Witkin et al. 2006) (Fig. 11.19). Chen et al. demonstrated preferential ischemia of the DCP in sickle cell retinopathy, which resulted in selective atrophy of the middle layers of the macula on SD-OCT (Chen et al. 2015).
Optical Coherence Tomography Angiography in Retinal Vascular Disease
Diabetic Retinopathy
In DR, OCTA shows microaneurysms as focally dilated capillaries contiguous with neighboring capillaries (Fig. 11.20). The visualization of microaneurysms can be enhanced by separating the vascular layers into SCP, MCP, and DCP, which enabled Choi et al. to determine that microaneurysms tend to be more detectable in the intermediate plexus (Huang et al. 2017; Choi et al. 2017).
OCTA is beneficial in cases where IRMAs may be confused with areas of NVE by assessing the level of these vessels with respect to the internal limiting membrane (ILM). En Face images of the SCP will identify IRMAs whereas images above the ILM will detect NV extending into the vitreous (de Carlo et al. 2016) (Fig. 11.21).
The advantage of OCTA over FA is that it consistently provides images that present a more accurate description of capillary non-perfusion, NV, and size of the FAZ because the image is not occluded by dye leakage (Al-Sheikh et al. 2016; Samara et al. 2017; Couturier et al. 2015). Images obtained by OCTA have the added advantage of separating retinal vessels into distinct layers (up to 3 in the macular area), which allows a more thorough examination of the effect of non-perfusion in each layer.
OCTA has also been helpful in understanding the contribution of the DCP to the oxygen requirements of the photoreceptor and outer retinal layers. Scarinci et al. found areas of capillary disruption in the DCP that corresponded to photoreceptor disruption on the SD-OCT, suggesting the importance of the DCP for the metabolic demand of the photoreceptors (Scarinci et al. 2016).
Retinal Vein Occlusion
Compared to FA, OCTA has the additional advantage of demonstrating the SCP and DCP with less interference of the retinal hemorrhage and dye leakage (Rispoli et al. 2015) (Fig. 11.22). Coscas et al. determined that, in RVO, the grayish non-perfused areas and the disrupted and dilated capillary network were more frequent in the DCP than the SCP (Coscas et al. 2016). This provides evidence that retinal vein occlusion affects the deeper plexus more severely than it affects the superficial plexus.
OCTA is also effective in the evaluation of the ischemic non-perfused areas in the retina, especially those involving the macula (Cardoso et al. 2016). This can be a very important prognostic tool in the prediction of visual recovery in some cases. Both Suzuki et al. and Chung et al. found that OCTA was superior in detecting eyes with capillary non-perfusion when compared to FA because it provided higher-resolution images (Suzuki et al. 2016; Chung et al. 2017). On the other hand, OCTA cannot detect non-perfused areas in the peripheral retina which are readily picked up by wide-field FA due to limited field of view (Suzuki et al. 2016).
Iida et al. used OCTA to challenge previously reported patterns of arteriovenous crossing in cases of BRVO by documenting a higher number of cases with venous overcrossing than FA was able to detect. They also noticed more venous narrowing and macular non-perfusion in these cases (Iida et al. 2017).
Retinal Artery Occlusion
Bonini Filho et al. (2015) described areas of non-perfusion in both SCP and DCP using OCTA. de Castro-Abeger et al. determined that OCTA was superior to FA in detecting perfusion defects in the SCP. This is due to the ability of OCTA to better visualize the vasculature in areas with retinal swelling (de Castro-Abeger et al. 2015).
Acute Macular Neuroretinopathy and Paracentral Acute Middle Maculopathy
Patients with AMN and PAMM present with hyperreflective retinal layers, thought to represent the effect of a retinal vascular insult. This hypothesis can be validated using OCTA by demonstrating areas of DCP defects (Pecen et al. 2015) (Fig. 11.23).
Sickle Cell Retinopathy
OCTA provides high-resolution images of the ischemic changes affecting the macula, which can shed light on the prognosis of visual affection and recovery in patients with sickle cell retinopathy. Minvielle et al. identified rarefied and dilated capillaries and enlargement of the FAZ in both SCP and DCP in all their patients with sickle cell retinopathy (Minvielle et al. 2016). They also noted capillary non-perfusion in the SCP of 72.2%, and in the DCP of 27.8% of their patients. Most capillary abnormalities were located in the temporal juxtafoveal region and might extend to the superior and inferior juxtafoveal regions.
In sickle cell retinopathy, OCTA can also be used to visualize abnormal NV developing at or around the optic disc as well as surrounding the macula. However, due to its limited access to the retinal periphery where most of the pathology is, wide-field FA remains superior to OCTA in the assessment of sickle cell retinopathy, especially in the proliferative stages.
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Fayed, A.E., Nesper, P.L., Fawzi, A.A. (2020). Imaging of Retinal Vascular Disease. In: Sheyman, A., Fawzi, A.A. (eds) Retinal Vascular Disease. Retina Atlas. Springer, Singapore. https://doi.org/10.1007/978-981-15-4075-2_11
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DOI: https://doi.org/10.1007/978-981-15-4075-2_11
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