Ophthalmic Surgery, Lasers and Imaging Retina

Case Report 

Localization of Paracentral Acute Middle Maculopathy Using Optical Coherence Tomography Angiography

Roy Schwartz, MD; Philip Hykin, FRCOphth; Sobha Sivaprasad, FRCOphth

Abstract

Paracentral acute middle maculopathy (PAMM) refers to band-like hyperreflective lesions seen on spectral-domain optical coherence tomography, mostly confined to the inner nuclear layer. It has been previously demonstrated to involve the deep capillary plexus (DCP) using optical coherence tomography angiography (OCTA). A 29-year-old female presented with PAMM and was investigated using a new OCTA system that shows not just the superficial capillary plexus and DCP, but also the four vascular plexuses as previously demonstrated in histology. Using this system, involvement of the DCP was shown, but also of more superficial layers, including the intermediate capillary plexus.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:619–624.]

Abstract

Paracentral acute middle maculopathy (PAMM) refers to band-like hyperreflective lesions seen on spectral-domain optical coherence tomography, mostly confined to the inner nuclear layer. It has been previously demonstrated to involve the deep capillary plexus (DCP) using optical coherence tomography angiography (OCTA). A 29-year-old female presented with PAMM and was investigated using a new OCTA system that shows not just the superficial capillary plexus and DCP, but also the four vascular plexuses as previously demonstrated in histology. Using this system, involvement of the DCP was shown, but also of more superficial layers, including the intermediate capillary plexus.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:619–624.]

Introduction

Paracentral acute middle maculopathy (PAMM) refers to band-like hyperreflective lesions as seen on spectral-domain optical coherence tomography (SD-OCT), which are mostly confined to the inner nuclear layer (INL) and are a result of ischemia of the intermediate and deep retinal capillary plexus.1–3 These lesions may occur in isolation, or in conjunction with other retinovascular conditions, including branch retinal artery occlusion (BRAO) and central retinal artery occlusion (CRAO), central retinal vein occlusion (CRVO), diabetic retinopathy, sickle cell retinopathy, and Purtscher retinopathy.4–6

Optical coherence tomography angiography (OCTA) is a novel and noninvasive technique for demonstrating the microvascular blood flow within the retina. It produces depth-resolved evaluation of the reflectance data from retinal tissue, providing a three-dimensional volume of information.7 Previous studies and case reports demonstrated OCTA findings seen in patients with PAMM, both at the level of the superficial vascular plexus (SCP), and the deep vascular plexus (DCP).8–18

En face structural OCT imaging is created from the three-dimensional reconstruction of rapidly acquired line scans. It provides segmented visualization of the various retinal and choroidal layers with depth-resolved precision.10 Using en face OCT evaluation, several studies demonstrated the benefit of this method to aid in the diagnosis of PAMM as well-described various distinctive patterns.10–12,18

In this case report, we aim to demonstrate OCTA and en face patterns using more accurate localization of the condition within the retinal vascular plexuses than demonstrated before in a patient with PAMM.

Case Report

A 29-year-old African-Caribbean female presented for an evaluation of acute onset fixed scotoma and intermittent flashes in her right eye (OD). She denied any symptoms in the left eye (OS). Her past medical history included chest infection for the previous 5 days, for which she was being treated with oral antibiotics. She denied use of oral contraceptives, sickle cell disease, or previous abortions. She confessed to exercising vigorously and not always hydrating properly. Her past ocular history and family history were unremarkable.

The patient's best-corrected visual acuity (BCVA) was 20/16 in both eyes (OU). Intraocular pressure was within normal limits, and anterior segment examination was unrevealing OU. Fundus examination OD showed tortuous and dilated veins, as well as few scattered intraretinal hemorrhages, suggestive of CRVO. SD-OCT identified a hyperreflective, band-like lesion located at the level of the INL consistent with PAMM (Figure 1A). Near-infrared image OD demonstrated a gray lesion the size of 1 disc area, nasal to the fovea (Figure 1B). Fundus autofluorescence showed mild hypoautofluorescence nasal to the fovea (Figure 1C).

Paracentral acute middle maculopathy (PAMM) in the right eye of a 29-year-old patient. (A) Spectral-domain optical coherence tomography shows a hyperreflective, band-like lesion located at the level of the inner nuclear layer consistent with PAMM. (B) Near-infrared image shows a gray lesion the size of 1 disc area, nasal to the fovea. (C) Fundus autofluorescence shows mild hypoautofluorescence nasal to the fovea.

Figure 1.

Paracentral acute middle maculopathy (PAMM) in the right eye of a 29-year-old patient. (A) Spectral-domain optical coherence tomography shows a hyperreflective, band-like lesion located at the level of the inner nuclear layer consistent with PAMM. (B) Near-infrared image shows a gray lesion the size of 1 disc area, nasal to the fovea. (C) Fundus autofluorescence shows mild hypoautofluorescence nasal to the fovea.

OCTA was performed using the Spectralis OCTA module (Heidelberg Engineering, Heidelberg, Germany). This system allows the demonstration of four vascular plexuses, as previously seen in histology: Nerve fiber layer vascular plexus (NFLVP), at the level of the nerve fiber layer (NFL); SCP, from the border of the NFL and the ganglion cell layer (GCL) to a point before the border of the inner plexiform layer (IPL) and INL; the inner capillary plexus (ICP), from that point to a point just after the IPL-INL border; and the DCP, from there to the end of the outer plexiform layer (OPL).19 At the level of the NFLVP layer, OCTA was unremarkable. En face OCT showed an area of hyperreflectivity mostly superonasal to the fovea (Figure 2A). In the SCP layer, two areas of hyporeflectivity were seen and corresponded to areas of hyperreflectivity on en face OCT (Figure 2B). The ICP layer demonstrated mild capillary dropout nasal to the fovea, but more substantial hyperreflective areas on en face OCT (Figure 2C). The DCP layer showed the largest area of capillary dropout of all layers. However, this distribution corresponded to a hyporeflective area on en face OCT, surrounded by an area of hyperreflectivity in its nasal aspect (Figure 2D).

Optical coherence tomography angiography (OCTA) examination of the right eye using the Heidelberg Spectralis OCTA module. (A) Level of the nerve fiber layer vascular plexus (NFLVP). Top left: OCTA image demonstrating vasculature at this level. Bottom left – segmentation of the NFLVP layer. Right – En face optical coherence tomography (OCT) showing an area of hyperreflectivity mostly superonasally to the fovea. (B) Level of the superficial capillary plexus (SCP). Top left: OCTA image at this level, demonstrating two areas of hyporeflectivity. Bottom left – segmentation of the SCP layer. Right – en face OCT showing areas of hyperreflectivity corresponding to the hyporeflective areas seen on OCTA, surrounded by further hyperreflectivity. (C) Level of the intermediate capillary plexus (ICP). Top left: OCTA image at this level, demonstrating some capillary dropout nasal to the fovea. Bottom left – segmentation of the ICP layer. Right – en face OCT showing an extensive area of hyperreflectivity nasal to the fovea. (D) Level of the deep capillary plexus (DCP). Top left: OCTA image at this level, demonstrating capillary dropout nasal to the fovea which is more significant than that seen at the ICP layer. Bottom left – segmentation of the DCP layer. Right – en face OCT showing an area of hyporeflectivity corresponding to the area with capillary dropout seen on OCTA, surrounded by an area of hyperreflectivity. (E) Level of the superficial vascular complex (SVC). Top left: OCTA image at this level, demonstrating a similar image to that seen at the level of the SCP. Bottom left – segmentation of the SVC layer. Right – en face OCT showing an area of hyperreflectivity resembling that seen at the SCP layer. (F) Level of the deep vascular complex (DVC). Top left: OCTA image at this level, demonstrating a similar image to that seen at the level of the DCP, albeit less pronounced. Bottom left – segmentation of the DVC layer. Right – en face OCT showing an area of hyperreflectivity more pronounced than at the level of the DCP.

Figure 2.

Optical coherence tomography angiography (OCTA) examination of the right eye using the Heidelberg Spectralis OCTA module. (A) Level of the nerve fiber layer vascular plexus (NFLVP). Top left: OCTA image demonstrating vasculature at this level. Bottom left – segmentation of the NFLVP layer. Right – En face optical coherence tomography (OCT) showing an area of hyperreflectivity mostly superonasally to the fovea. (B) Level of the superficial capillary plexus (SCP). Top left: OCTA image at this level, demonstrating two areas of hyporeflectivity. Bottom left – segmentation of the SCP layer. Right – en face OCT showing areas of hyperreflectivity corresponding to the hyporeflective areas seen on OCTA, surrounded by further hyperreflectivity. (C) Level of the intermediate capillary plexus (ICP). Top left: OCTA image at this level, demonstrating some capillary dropout nasal to the fovea. Bottom left – segmentation of the ICP layer. Right – en face OCT showing an extensive area of hyperreflectivity nasal to the fovea. (D) Level of the deep capillary plexus (DCP). Top left: OCTA image at this level, demonstrating capillary dropout nasal to the fovea which is more significant than that seen at the ICP layer. Bottom left – segmentation of the DCP layer. Right – en face OCT showing an area of hyporeflectivity corresponding to the area with capillary dropout seen on OCTA, surrounded by an area of hyperreflectivity. (E) Level of the superficial vascular complex (SVC). Top left: OCTA image at this level, demonstrating a similar image to that seen at the level of the SCP. Bottom left – segmentation of the SVC layer. Right – en face OCT showing an area of hyperreflectivity resembling that seen at the SCP layer. (F) Level of the deep vascular complex (DVC). Top left: OCTA image at this level, demonstrating a similar image to that seen at the level of the DCP, albeit less pronounced. Bottom left – segmentation of the DVC layer. Right – en face OCT showing an area of hyperreflectivity more pronounced than at the level of the DCP.

A slab named the superficial vascular complex (SVC), roughly corresponding to the SCP in other OCTA machines (from the internal limiting membrane to before the IPL-INL border) showed an image that was similar to that seen at the SVP layer (Figure 2E). A slab named deep vascular complex (DVC), from before the IPL-INL border to the end of the OPL, corresponding roughly to the deep capillary plexus in other OCTA machines, demonstrated OCTA findings that were somewhat similar to those seen at the DCP level, albeit with more pronounced hyperreflectivity on en face OCT (Figure 2F).

OCTA was also performed on the AngioPlex OCTA system (Carl Zeiss Meditec, Dublin, CA). Some minor alterations in vessel density were seen at the level of the SCP nasal to the fovea. En face OCT demonstrated a large hyperreflective area nasal to the fovea, which was similar in size and shape to that seen on the Heidelberg system at the SCP level, albeit more hyperreflective (Figure 3A). At the level of the DCP, vessel density alteration nasal to the fovea was more marked than in the SCP level, resembling capillary nonperfusion. The en face OCT demonstrated a nonconfluent hyperreflective area nasal to the fovea that was similar in size to that seen at the SCP level. However, hyperreflectivity at this level lacked similarity to that seen on the Heidelberg system at the DCP level, both in shape and in size (Figure 3B).

Optical coherence tomography angiography (OCTA) examination of the right eye using the Zeiss AngioPlex system. (A) Level of the superficial capillary plexus (SCP). Top left – OCTA image at this level, showing some minor alterations in vessel density. Bottom left – segmentation of the SCP layer. Right – en face optical coherence tomography (OCT) image showing a large hyperreflective area nasal to the fovea, similar to the size and shape of that seen on the Heidelberg system at the SCP level. (B) Level of the deep capillary plexus (DCP). Top left – OCTA image at this level, showing more marked capillary dropout nasal to the fovea. Bottom left – segmentation of the DCP layer. Right – en face OCT image showing a non-confluent hyperreflective area nasal to the fovea similar in size to that seen at the level of the SCP, but not similar to that seen at the DCP level with the Heidelberg system.

Figure 3.

Optical coherence tomography angiography (OCTA) examination of the right eye using the Zeiss AngioPlex system. (A) Level of the superficial capillary plexus (SCP). Top left – OCTA image at this level, showing some minor alterations in vessel density. Bottom left – segmentation of the SCP layer. Right – en face optical coherence tomography (OCT) image showing a large hyperreflective area nasal to the fovea, similar to the size and shape of that seen on the Heidelberg system at the SCP level. (B) Level of the deep capillary plexus (DCP). Top left – OCTA image at this level, showing more marked capillary dropout nasal to the fovea. Bottom left – segmentation of the DCP layer. Right – en face OCT image showing a non-confluent hyperreflective area nasal to the fovea similar in size to that seen at the level of the SCP, but not similar to that seen at the DCP level with the Heidelberg system.

Discussion

This report demonstrates the different patterns as seen on OCTA and en face OCT in the different vascular plexuses corresponding to histological classification in a patient with PAMM. To the best of our knowledge, this is the first reported work to describe such findings.

Using the Heidelberg machine, we could demonstrate a difference in findings between the four different vascular layers. Interestingly, the layer with the most visible change on OCTA was the DCP layer. Similar changes were seen at the level of the DVC. This is not surprising, as the DVC engulfs in it the DCP. Changes were also seen in the ICP and SVP layers, and, to a lesser extent, also in the NFLVP layer, although in the latter changes were confined to the en face image only.

Most previous studies reported mostly changes at the DCP level in PAMM patients. However, some studies also reported changes at superficial layers. In a study by Nemiroff et al. conducted on eight patients with PAMM, the SCP demonstrated minimally attenuated perfusion in some of the affected eyes.8 In a study by Sridhar et al. on 16 patients with PAMM, variable areas of capillary dropout within the SCP and DCP in the area corresponding to the PAMM lesions were seen.12 A case report by Trese et al. on a patient with PAMM secondary to primary antiphospholipid syndrome also described perfusion deficits at the SCP, as well as the DCP.20

In the region of the central macula, the capillary plexuses exist within a superficial, intermediate, and deep triplanar system.19,21 The superficial system resides predominantly within the GCL and to a lesser extent within the NFL. The deeper system is composed of an ICP layer, located along the inner portion of the INL at the IPL border, and a DCP within the outer portion of the INL bordering the OPL. The Heidelberg OCTA system largely replicates this histological configuration (Figure 4). With this breakdown, it is clear that both the ICP and the DCP show changes on OCTA and on en face OCT, although OCTA changes were more pronounced at the level of the DCP. En face OCT findings were pronounced at both levels.

Localization of the different vascular plexuses in the macula with the Heidelberg optical coherence tomography angiography (OCTA) system, corresponding to histological vascular plexuses. The nerve fiber layer vascular plexus (NFLVP) is in the nerve fiber layer (NFL). The superficial capillary plexus (SCP) stretches from the border of the NFL and the ganglion cell layer (GCL) to a point before the inner plexiform layer (IPL) and inner nuclear layer (INL). The intermediate capillary plexus (ICP) spans from that point to a point just after the IPL-INL border. The deep capillary plexus (DCP) starts at that point and ends at the end of the outer plexiform layer (OPL). The superficial vascular complex (SVC), roughly corresponding to the superficial capillary plexus in other OCTA machines, includes within it the NFLVP and SCP layers. The deep vascular complex (DVC), corresponding roughly to the DCP in other OCTA machines, includes within it the ICP and DCP. ONL = outer nuclear layer.

Figure 4.

Localization of the different vascular plexuses in the macula with the Heidelberg optical coherence tomography angiography (OCTA) system, corresponding to histological vascular plexuses. The nerve fiber layer vascular plexus (NFLVP) is in the nerve fiber layer (NFL). The superficial capillary plexus (SCP) stretches from the border of the NFL and the ganglion cell layer (GCL) to a point before the inner plexiform layer (IPL) and inner nuclear layer (INL). The intermediate capillary plexus (ICP) spans from that point to a point just after the IPL-INL border. The deep capillary plexus (DCP) starts at that point and ends at the end of the outer plexiform layer (OPL). The superficial vascular complex (SVC), roughly corresponding to the superficial capillary plexus in other OCTA machines, includes within it the NFLVP and SCP layers. The deep vascular complex (DVC), corresponding roughly to the DCP in other OCTA machines, includes within it the ICP and DCP. ONL = outer nuclear layer.

Previous papers have suggested that both the ICP and DCP are involved in the pathogenesis of PAMM. In a review paper by Rahimy et al.,3 the authors mention that PAMM has been traditionally attributed to ischemia of the DCP, but that they cannot exclude a contributing role from the overlying ICP given that this plexus resides immediately superficial to the PAMM lesion on SD-OCT. They conclude by saying that distinguishing the intermediate and deep networks even with recent advancements in technology such as OCTA has proven to be challenging. In this paper, we suggest that with modern OCTA technology, such a separation is possible, and demonstrates an involvement of the ICP as well as the DCP, although to a lesser extent, as judged by the OCTA component of the image. This is plausible, as anatomically it is conceivable that the INL may receive its blood supply predominantly from the proximal ICP, whereas the OPL may receive its blood supply predominantly from the proximal DCP.3

As shown in previous studies, our case demonstrated distinct findings on en face OCT. Sridhar et al. classified PAMM in eyes with retinal arterial and venous occlusion into three distinct patterns: Arteriolar (mirroring the distribution of large retinal arterioles), globular (around distal capillaries), and fern-line (along the retinal veins).12 Our case seems to fit the arteriolar pattern. In their study, cases demonstrating the arteriolar pattern suffered from BRAO, CRAO, or CRVO combined with cilioretinal artery occlusion. Our patient did not show signs of arterial occlusion. In their article, Sridhar et al. suggested that even in the absence of a true BRAO, the transient occlusion of a large retinal arteriole with rapid restoration of normal flow could induce ischemia in the watershed zone of the middle retina.12 This hypothesis possibly applies to our case. We suggest that a possible transient ischemic event at the arteriolar level has led to middle-retinal ischemia, giving an arteriolar pattern on en face OCT. Although in the past, such events may have been missed, the availability of en face imaging provides a sensitive method for detection of such short-lived events.

Our case showed differences in the en face pattern between the two OCTA machines at the levels of the SCP and DCP. This may be explained by the different segmentation as done by the two machines. In the Angioplex machine, the SCP is defined by the ILM as the inner surface, and an approximation of the IPL as the outer surface, as estimated by the location of the ILM plus 70% of the thickness between the ILM and OPL. The DCP slab is defined by the IPL as the inner surface, and the OPL, as approximated by the retinal pigment epithelium minus 110 μm, as the outer surface.22 In the Heidelberg system, the device delineates the layers automatically and uses the conventions described above for layer segmentation. Another reason may be the different algorithms employed by the different systems.

In conclusion, this case demonstrated the possible involvement of the ICP in the pathogenesis of PAMM. As OCTA technology continues to evolve, more studies may help to shed light on these findings using more patients.

References

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Authors

From NIHR Biomedical Research Centre, Moorfields Eye Hospital, London, UK.

Dr. Hykin reports grants, personal fees, and non-financial support from Bayer, Novartis, and Allergan outside the submitted work. Dr. Sivaprasad reports grants and personal fees from Bayer, Novartis, and Allergan; grants and personal fees from Boehringer Ingelheim; and personal fees from Heidelberg Engineering outside the submitted work. Dr. Schwartz reports no relevant financial disclosures.

Address correspondence to Roy Schwartz, MD, NIHR Biomedical Research Centre, Moorfields Eye Hospital, 162 City Road, London, EC1V 2PD, United Kingdom; email: royschwartz@gmail.com.

Received: September 24, 2017
Accepted: January 22, 2018

10.3928/23258160-20180803-10

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