Clinical science

Br J Ophthalmol: first published as 10.1136/bjophthalmol-2019-315443 on 6 May 2020. Downloaded from http://bjo.bmj.com/ on May 11, 2020 at Uppsala Universitet BIBSAM Consortia.
Henle fibre layer haemorrhage: clinical features
and pathogenesis
Caroline R Baumal ‍ ‍,1 David Sarraf,2 Tara Bryant,1 Wei Gui,2 Nora Muakkassa,1
Francesco Pichi ‍ ‍,3 Giuseppe Querques ‍ ‍,4 Netan Choudhry,5 Mehmet Yasin Teke,6
Andrea Govetto ‍ ‍,7 Alessandro Invernizzi ‍ ‍,8 Dean Eliott,9 Alain Gaudric,10
Eduardo Cunha de Souza,11 Jonathan Naysan,12 Andrea Lembo,3 Grace C Lee,13
K Bailey Freund14

For numbered affiliations see Abstract The oblique orientation of Henle fibres accounts
end of article. Background To describe the clinical presentation for changes in OCT reflectivity when the HFL is
and characteristic imaging features of deep retinal imaged with an off-­axis OCT entry beam in normal
Correspondence to eyes.2 3 Haemorrhage in HFL displays a character-
haemorrhages primarily located in the Henle fibre layer
Dr Caroline R Baumal,
Ophthalmology, New England (HFL) of the macula. The spectrum of aetiologies and a istic radial pattern of blood and has recently been
Eye Center, Boston, MA 02111, comprehensive theory of pathogenesis are presented. described in association with macular telangiectasia
USA; c​ baumal@​gmail.​com Methods This is a retrospective, multicentre case series (Mac Tel) type 2.4 5 OCT demonstrating haemor-
evaluating eyes with retinal haemorrhage in HFL. Clinical rhage at the level of HFL is a distinctive imaging
Received 23 December 2019
Revised 6 April 2020 features, underlying aetiology, systemic and ocular risk finding. The source of the blood likely originates
Accepted 8 April 2020 factors, visual acuity, and multimodal imaging including from the deep retinal capillary plexus (DCP) in Mac
fundus photography and cross-­sectional and en face Tel type 2 as it is positioned adjacent to the HFL.6–8
optical coherence tomography (OCT) are presented. The DCP has recently been shown to be the major
Results Retinal haemorrhages localised to HFL in 33 level of venous outflow for the retinal capillary
eyes from 23 patients were secondary to acute blunt plexus, and this arrangement may provide clue to

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trauma to the head (n=2), eye (n=1) and trunk (n=1), the aetiology of haemorrhage in HFL.9 10
ruptured intracranial aneurysm (Terson’s syndrome, This report presents the largest case series with
n=3), general anaesthesia (n=1), epidural anaesthesia radial haemorrhage tracking in HFL. The associated
(n=1), hypertension with anaemia (n=1), decompression features are described with advanced retinal imaging
retinopathy (n=1), postvitrectomy with intraocular gas including cross-­sectional and en face OCT, and the
(n=1), retinal vein occlusion (n=7), myopic degeneration common pathogenic mechanisms that lead to this
(n=2), macular telangiectasia type 2 (n=1), and interesting presentation are presented. The authors
polypoidal choroidal vasculopathy (n=1). Defining propose the terminology ‘Henle fiber layer hemor-
clinical features included deep retinal haemorrhage with rhage (HH)’ to describe this characteristic pattern
feathery margin and petaloid pattern radiating from the based on OCT anatomical localisation of the haem-
fovea. OCT demonstrated characteristic hyper-­reflectivity orrhage that occurs in this multifactorial disorder.
from the haemorrhage delineated by obliquely oriented
fibres in the Henle layer. Spontaneous resolution of HFL
Methods
haemorrhage occurred after 3 months in 15 patients
In this retrospective, multicentre case series, retinal
with follow-­up.
specialists from multiple international centres were
Conclusion The characteristic petaloid-­shaped,
surveyed to search their databases for cases with
deep intraretinal haemorrhage with a feathery margin
retinal haemorrhage localising to the HFL on clin-
localised to HFL is associated with various disorders.
ical examination and OCT.
The terminology ’Henle fiber layer hemorrhage (HH)’
Detailed chart review was performed and
is proposed to describe the clinical and OCT findings,
de-­identified data were collected, including patient
which may result from abnormal retinal venous pressure
age, gender, concomitant systemic and ocular disor-
from systemic or local retinovascular disorders affecting
ders, medications, baseline and when available final
the deep capillary plexus or from choroidal vascular
Snellen visual acuity, findings of clinical exam-
abnormalities.
ination, and analysis of retinal imaging including
fundus photography and cross-­ sectional and en
© Author(s) (or their face spectral-­domain OCT (Heidelberg Spectralis,
employer(s)) 2020. No Introduction Germany, or Cirrus, Carl Zeiss Meditec, Dublin,
commercial re-­use. See rights
and permissions. Published The distinctive arrangement of Henle fibres around California). Macular raster scans were performed
by BMJ. the fovea was surmised based on clinical findings, at the physician’s discretion and included a volume
such as with the appearance of a macular star cube through the fovea. OCT and fundus images
To cite: Baumal CR, Sarraf D,
formed by lipid exudate, as well as by pathological were evaluated by two authors (CRB, DS) to
Bryant T, et al.
Br J Ophthalmol Epub ahead studies. The ability to identify and study the Henle confirm the presence of the characteristic HFL
of print: [please include Day fibre layer (HFL) and the details of the retinal haemorrhage. Features of HFL haemorrhage evalu-
Month Year]. doi:10.1136/ anatomical layers in vivo has been greatly enhanced ated from clinical images included laterality, multi-
bjophthalmol-2019-315443 by optical coherence tomography (OCT) imaging.1 centricity, shape, location and pattern. On OCT,
Baumal CR, et al. Br J Ophthalmol 2020;0:1–7. doi:10.1136/bjophthalmol-2019-315443 1
Clinical science

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Table 1 Clinical features of eyes presenting with Henle fibre layer haemorrhage (HH)
Presenting VA in Final VA in
Case Mechanism Aetiology Laterality of HH affected eye(s) affected eye(s) Length of follow-­up/sequelae
1 Head trauma, blunt. CVP OU 20/30, 20/15 20/20, 20/20 6 weeks, resolving HH.
Intracranial haemorrhage. AMN.
Parietal fracture. Ellipsoid loss.
2 Head trauma, blunt. CVP OU 20/40, 20/30 20/20, 20/20 4 weeks, resolved HH after SAH drainage.
SAH.
Elevated ICP.
Papilloedema requiring surgical drainage.
3 Trunk trauma, severe compression. CVP OU 20/200, 20/200 NA  NA
4 SAH. CVP OU 20/400, 20/150 20/40, 20/30 12 weeks, resolved HH.
S/P coil embolisation under GA. Ellipsoid loss.
5 SAH. CVP OU 20/400, 20/400 NA NA
S/P coil embolisation under GA.
6 SAH. CVP OU 20/20, CF NA NA
7 Elevated CVP during uncomplicated GA or Valsalva during CVP OU 20/30, 20/25 20/20, 20/20 4 weeks, resolved HH.
intubation/extubation.
8 Epidural anaesthesia for spinal procedure with postprocedural CVP OU 20/25, 20/25 20/20, 20/20 52 weeks, resolved HH, mild scotoma.
CSF leak.
9 Uncontrolled hypertension. CVP OU 20/70, 20/80 20/25, 20/25 NA
Anaemia.
10 Decompression retinopathy S/P Visian intraocular contact lens RV OU 20/20, 20/25 20/20, 20/25 10 weeks, resolved HH.
surgery OU.
Myopic degeneration (−17D).
11 Ocular trauma, blunt impact OS. RV OS 20/20, 20/40 20/20, 20/20 3 weeks, resolved HH.
No sequelae.
12 Day 1 S/P PPV, ILM peel, phacoemulsification, PCIOL, 25% SF6 RV OS CF with intraocular gas 20/80 3 weeks, resolving HH.
gas with face-­down position for 12 hours.
13 CRVO with PAMM. RV OD 5/200 CF 52 weeks, resolved HH, thin retina.
14 BRVO, no CME. RV OD 20/20 20/20 NA
HTN, POAG.

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15 BRVO, no CME. RV OD 20/20 20/50 20 weeks, developed CME that resolved
HTN. after anti-­VEGF injection.
16 BRVO, no CME. RV OD 20/20 20/20 28 weeks, developed CME that resolved
HTN, obese. after anti-­VEGF.
17 BRVO, no CME. RV OD 20/40 20/100 4 years, developed CME.
18 BRVO, CME. RV OS 20/30 NA NA
19 BRVO. RV OS 20/30 20/20 2 years.
20 Mac Tel type 2 with CNV. RV OD 2/200 4/200 10 years.
Macular fibrosis.
21 PCV (also known as aneurysmal type 1 neovascularisation) OD. SR OD 20/250 20/60 8 weeks.
Uncontrolled HTN. Resolved HH.
22 Myopic degeneration, peripapillary atrophy. SR OD 20/200 NA NA
No CNV.
23 Myopic degeneration (−15D), posterior staphyloma, new lacquer SR OS 20/400 20/80 12 years.
crack. Resolved HH.
22 weeks pregnant.
No CNV.
AMN, acute macular neuroretinopathy; BRVO, branch retinal vein occlusion; CF, count finger vision; CME, cystoid macular oedema; CNV, choroidal neovascularisation; CRVO, central retinal vein occlusion; CSF,
cerebrospinal fluid; CVP, central venous pressure; GA, general anaesthesia; HTN, hypertension; ICP, intracranial pressure; ILM, internal limiting membrane; NA, not available; OD, right eye; OS, left eye; OU, both eyes;
PAMM, paracentral acute middle maculopathy; PCIOL, posterior chamber intraocular lens; PCV, polypoidal choroidal vasculopathy; POAG, primary open angle glaucoma; PPV, pars plana vitrectomy; RV, retinovascular;
SAH, subarachnoid haemorrhage; SF6, sulfahexafluoride ; S/P, status post; SR, subretinal; Mac Tel, macular telangiectasia; VA, visual acuity; VEGF, vascular endothelial growth factor.

HFL retinal haemorrhage was defined as hyper-­reflective mate- haemorrhage to HFL. Table 1 summarises the characteristics of
rial in the HFL of the macula that colocalised with deep retinal the patients and the causes of HFL haemorrhage. There were 10
haemorrhage in the fundus image. OCT features at presentation men and 13 women, ranging from 15 to 77 years of age. Visual
and follow-­up when available were assessed. The presence of acuity in the affected eye at presentation ranged from 20/20 to
associated preretinal and/or subretinal haemorrhage or other finger counting. Ten of the cases demonstrated bilateral HFL
OCT abnormalities was also assessed. En face OCT (Cirrus, haemorrhage, and the underlying aetiologies in these cases were
Carl Zeiss Meditec, or Optovue, Fremont, California) was also severe blunt trauma to the head and trunk, intracranial aneu-
performed in select cases with segmentation at the HFL level rysm, general and epidural anaesthesia, systemic hypertension
confirming the location of blood and the characteristic radial with anaemia, and decompression retinopathy. In the remaining
pattern extending from the fovea. 13 cases where HFL haemorrhage was unilateral, the underlying
causes were local retinovascular or choroidal vascular disorders,
Results affecting the right eye in eight cases and the left eye in five cases.
Twenty-­three cases were contributed from 14 retina practices. The mechanism of HFL haemorrhage based on history and
For two cases (cases 15 and 20), only clinical fundus photo- clinical presentation was attributable to the following aetiolo-
graphs were submitted as OCT was not commercially avail- gies: increased systemic central venous pressure in 9 of the 10
able at the time of patient presentation. For the remaining bilateral cases (intracranial haemorrhage from trauma or aneu-
21 cases, review of OCT confirmed localisation of the retinal rysm, trunk trauma, general anaesthesia, Valsalva, epidural
2 Baumal CR, et al. Br J Ophthalmol 2020;0:1–7. doi:10.1136/bjophthalmol-2019-315443
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Figure 2 Case 13. A middle-­aged woman with Henle fibre layer
haemorrhage and CRVO associated with PAMM. Colour fundus
photograph (A) revealing petaloid-­shaped, deep retinal haemorrhages
Figure 1 Case 1. Henle fibre layer haemorrhage after blunt head radiating from the fovea in her right eye with CRVO. Overlay of the
trauma with intracranial haemorrhage in a middle-­aged man. Colour retinal veins imaged with OCT angiography on the colour fundus
fundus photograph (A: right eye; B: left eye) at presentation illustrates image (B) with green cursor marking the venules of the DCP. Overlay
petaloid, deep retinal haemorrhages radiating from the fovea of en face of the DCP on the colour fundus image (C) and the green
responsible for self-­reported red, flower-­shaped scotomas. En face OCT cursor confirms the colocalisation of venules of the DCP with the en
(inset in A and B) segmented at the outer plexiform layer confirms the face hyper-­reflective PAMM lesions. Cross-­sectional OCT (D) illustrates
HFL location. Cross-­sectional OCT (C: right eye; D: left eye) illustrates foveal HFL haemorrhage (yellow circle) with adjacent PAMM lesions
hyper-­reflectivity and subtle oblique striations in HFL. At follow-­up 6 (yellow arrowheads). DCP, deep capillary plexus; HFL, Henle fibre layer;
weeks later, cross-­sectional OCT displays a hyper-­reflective vertical line OCT, optical coherence tomography; PAMM, paracentral acute middle
in the right fovea (E) and bilateral perifoveal ellipsoid loss (E and F). maculopathy.
HFL, Henle fibre layer; OCT, optical coherence tomography.

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anaesthesia, hypertension), increased local retinal venous pres- neuroretinopathy (AMN) and case 13 (figure 2) displayed para-
sure in 10 cases (branch retinal vein occlusion (BRVO), central central acute middle maculopathy (PAMM). Both of these disor-
retinal vein occlusion (CRVO), status post pars plana vitrectomy, ders have been implicated to result from flow deficits in the DCP,
decompression retinopathy, local eye trauma), localised abnor- especially PAMM.11–19 The association of PAMM and AMN
mality of the DCP in 1 case (Mac Tel type 2) and subretinal with HFL haemorrhage, in which the haemorrhage is presumed
bleeding in 3 cases (polypoidal choroidal vasculopathy (PCV), to originate from the DCP in cases of elevated local or systemic
myopic degeneration, exudative age-­related macular degenera- venous pressure, is therefore a consistent relationship.
tion). The majority of cases (cases 1 through 20) had a char-
acteristic petaloid pattern of deep retinal haemorrhage with a Brief description of two cases
feathery margin (figures 1A, B, 2A and 3), presumably origi- Case 1
nating from the DCP with blood tracking through the adjacent A Caucasian man with no medical history was found unrespon-
HFL to produce this appearance. Outside of the macular region, sive following blunt head trauma from a fist fight, with secondary
the associated deep retinal haemorrhage invariably displayed a intracranial haemorrhage. On regaining consciousness, he
rounder shape (figures 1A, B and 2A). Preretinal or inner retinal complained of bilateral ‘red flower’-shaped scotomas. Vision
haemorrhage was also noted in four cases, including three cases was 20/30 on the right eye and 20/15 on the left eye. Fundu-
with intracranial haemorrhage from an intracranial aneurysm (as scopic examination demonstrated bilateral petaloid-­ shaped,
in figure 3A,B) and one case after complicated epidural anaes- deep retinal haemorrhages in a radiating pattern from the fovea
thesia (figure 3C,D). In three cases due to myopic degeneration (figure 1A and B). OCT localised the haemorrhages to HFL in
(cases 21 and 22) and PCV (case 23), there was elevated subret- a characteristic pattern (figure 1C and D). The HFL haemor-
inal haemorrhage in the fovea surrounded by haemorrhage in rhages spontaneously improved after 6 weeks and visual acuity
HFL, likely the result of breakthrough of the blood from the returned to baseline with mild residual scotoma. Follow-­up OCT
associated choroidal neovascular membrane (figure 3F). revealed bilateral perifoveal ellipsoid loss (figure 1E and F) and
In 15 cases where follow-­up was available, spontaneous reso- a vertical hyper-­reflective line in the right fovea (figure 1E). The
lution of HFL haemorrhages was noted within 3 months of subsequent finding of ellipsoid zone and outer nuclear layer loss
presentation. In three cases (cases 1, 4 and 10), ellipsoid zone may be attributed to injury from the initial blunt trauma with
disruption was noted on the follow-­ up OCT at 6–12 weeks photoreceptor disruption, secondary to HFL haemorrhage or as
post presentation (figure 1E and F). In four cases (cases 1, 4, a result of trauma-­induced AMN.12
10 and 13), a hyper-­reflective vertical line, as seen in figure 1E,
was noted in the centre of the fovea on resolution of the haem- Case 13
orrhage, which may represent an OCT feature signifying prior A middle-­aged woman presented with acute vision loss in
HFL haemorrhage. the right eye measuring counting fingers. Retinal examina-
In addition to haemorrhage in HFL, two cases displayed addi- tion demonstrated scattered petaloid retinal haemorrhages
tional OCT findings consistent with specific DCP disorders. and mildly dilated and tortuous retinal veins, consistent with
Case 1 (figure 1) demonstrated OCT features of acute macular CRVO on the right eye (figure 2A). OCT angiography (OCTA)
Baumal CR, et al. Br J Ophthalmol 2020;0:1–7. doi:10.1136/bjophthalmol-2019-315443 3
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Figure 4 OCT from selected cases with Henle fibre layer haemorrhage
(HH). Case 2: a young man with HH due to blunt head trauma. Cross-­
sectional OCT (A: right eye; B: left eye) reveals hyper-­reflective deep
retinal haemorrhage radiating in HFL in the characteristic segmented
pattern. Associated fundus autofluorescence images also show the
distinctive petaloid and radial pattern of the blood. Case 9: HH in a
patient with uncontrolled hypertension and anaemia. OCT (C: right eye;
D: left eye) shows hyper-­reflective deep retinal haemorrhage radiating
in HFL with the characteristic segmented pattern. Registered near
infrared images display the petaloid radiating haemorrhages. Case
14: BRVO with HH nasal to the fovea. OCT (E) shows hyporeflective
oblique lines partitioning the characteristic hyper-­reflective HH with
scan location shown on the adjacent fluorescein angiogram image.
Case 19: BRVO with hyper-­reflective haemorrhage (F) radiating in HFL
in the characteristic segmented pattern separated by hyporeflective

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oblique lines. Registered near infrared image displays the level of
the corresponding OCT and shows the haemorrhage with feathery
edges. Case 23: HH due to polypoidal choroidal vasculopathy with
characteristic hyper-­reflective haemorrhage at the HFL level separated
by the hyporeflective lines on cross-­sectional OCT (G). Note the polyp
Figure 3 Colour fundus images of cases illustrating the three (H) adjacent to HH. Registered near infrared images reveal feathery
mechanisms of Henle fibre layer haemorrhage. Case 6 (A and B) margin of haemorrhage in HFL. BRVO, branch retinal vein occlusion; HFL,
shows bilateral petaloid, deep perifoveal retinal haemorrhages with Henle fibre layer; OCT, optical coherence tomography.
feathery margins secondary to elevated central venous pressure
from subarachnoid haemorrhage with Terson’s syndrome. Preretinal
haemorrhage is also present. Case 8 (C and D) shows bilateral radiating a petaloid or radial distribution within the fovea. Outside of the
petaloid haemorrhages after epidural anaesthetic with cerebrospinal fovea where the HFL orientation is vertical and not radial, blood
fluid leak due to elevated central venous pressure. Case 12 (E) shows in HFL exhibited a deep round morphology. Cross-­sectional and
resorbing radial haemorrhage in HFL resulting from increased retinal en face OCT confirmed the localisation of the level of haem-
venous pressure secondary to face-­down positioning and intraocular gas orrhage to HFL and illustrated a characteristic hyper-­reflective
expansion after vitrectomy for macular hole. This image was obtained pattern that is a signature OCT finding for this presentation
2 weeks postvitrectomy after resorption of intraocular gas. Case 23 (F) (figure 4A, B, C, D, E, F, G H). Hyporeflective oblique septae,
with radial haemorrhage in HFL adjacent to subretinal haemorrhage in which may represent Henle fibres coursing through the haemor-
the fovea from high myopia with type 2 choroidal neovascularisation. rhage, were noted to subdivide the hyper-­reflective blood in HFL
into segments (figure 4B, C, E, F G). Petaloid haemorrhages with
or without feathery borders were typical of systemic disorders
shows the retinal veins (green cursor) of the DCP overlaid on with high central venous pressure such as Terson’s syndrome,
the colour fundus image (figure 2B). Overlay of en face OCT but were also noted in a case of CRVO and were often associ-
on the colour fundus image (figure 2C) confirms colocalisation ated with peripheral deep round spots of haem. Local causes
of venules of the DCP (green cursor) with the en face hyper-­ of haemorrhage in HFL typically displayed a radial or feathery
reflective PAMM lesions. OCT illustrated foveal haemorrhage configuration of blood and were associated with either retino-
in HFL and multifocal PAMM lesions in a fern-­like perivenular vascular abnormalities or choroidal vascular disorders. Based on
distribution (figure 2D). After 1 year, vision was unimproved, OCT localisation, the characteristic pattern and the association
with attenuation of the inner nuclear layer (INL) and a central with multiple disorders, we propose that this clinical presenta-
hyper-­reflective vertical line in the fovea on OCT. tion be referred to as Henle fiber layer hemorrhage (HH), which
implies a specific pattern, pathoanatomy and mechanism of
Discussion development.
The cases described in this series all displayed a distinctive pattern The HFL comprised long, cylindrical, unmyelinated cone and
of deep, radial retinal haemorrhage in the macula localised to rod axons which synapse in the outer plexiform layer (OPL)
HFL. Specific features were notable related to the anatomy of and are radially orientated around the fovea due to the embry-
the HFL, including a feathery edge of the HFL haemorrhage and ological development of the foveal pit.20–22 The inner fibres of
4 Baumal CR, et al. Br J Ophthalmol 2020;0:1–7. doi:10.1136/bjophthalmol-2019-315443
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Systemic aetiologies of increased venous pressure were noted
Table 2 Aetiology and mechanism of Henle fibre layer haemorrhage
in 9 of 10 patients presenting with bilateral HFL haemorrhage
(HH)
(cases 1–9), and included blunt trauma, intracranial haemorrhage,
Description Aetiology Terson’s syndrome, status post general and epidural anaesthesia,
HH features: Elevated central venous pressure: Valsalva retinopathy, and acute systemic hypertension. In cases
►► Deep retinal haemorrhage ►► Terson’s syndrome of Terson’s syndrome (cases 4, 5 and 6) and brain trauma (cases
►► Feathered margin ►► Valsalva manoeuvre 1 and 2), an acute rise in intracranial pressure may lead to retinal
►► Petaloid shape ►► Trauma
venous hypertension due to the sudden effusion of cerebrospinal
►► Radial orientation ►► Epidural injection
►► Pericentral ►► Whiplash maculopathy fluid into the optic nerve sheath compressing the central retinal
►► General anaesthesia vein and increasing venous backflow.31 Abrupt fluctuations in
  Elevated local venous pressure (retinovascular): intracranial venous pressure may also occur during general
►► Retinal vein occlusion (branch or central) anaesthesia or with epidural injections.32–34 Valsalva manoeuvres
►► Decompression maculopathy can also induce rapid changes in intracerebral blood flow from
►► Blunt globe trauma the mechanical effects of increased intrathoracic pressure and
►► Face-­down positioning and expansile gas autonomic compensatory activity, leading to elevated central
postvitrectomy
venous pressure.35 36
►► Macular telangiectasia type 2
Local causes leading to HFL haemorrhage included retino-
  Choroidal vascular:
►► Polypoidal choroidal vasculopathy vascular disorders, of which seven cases resulted from retinal
(also referred to as aneurysmal type 1 vein occlusion. Interestingly, one case of CRVO displayed
neovascularisation) concomitant PAMM lesions in association with the HFL haem-
►► Neovascular age-­related macular orrhage. The association of PAMM and HFL layer haemorrhage
degeneration is not surprising given the common underlying pathoanatomy
►► Myopic degeneration±type 2 choroidal
involving the DCP. OCTA has demonstrated that the DCP is
neovascularisation
the primary level of pathoanatomical abnormality in BRVO and
may be at greatest risk of bleeding due to venous pressure fluc-
tuation.10 37 An additional case was described of a patient with
Muller cell glia also course through HFL.23 The oblique orien- radial HFL haemorrhage on the first postoperative day of head-­
tation of fibres in HFL coursing at an angle accounts for the down positioning for macular hole surgery presumably due to

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petaloid or teardrop shape of the retinal haemorrhage as well increased retinal venous pressure from the local effects of gas
as the feathery margins notable in our series (figure 3A, B, C, tamponade. Finally, a case of Mac Tel type 2 and HFL haem-
D, E F). This distinctive orientation of HFL also explains the orrhage was also included in this study. Prior published cases of
macular star pattern of exudation described in neuroretinitis radial haemorrhage in association with Mac Tel have exclusively
and hypertension.2 In addition to exudates, other materials may affected the right eye, including the Mac Tel case in this study.4
radialise in the HFL. Dissociated pigment in age-­related macular While this may be strictly coincidental, it is interesting to note
degeneration has been noted to track in the HFL and has been the unique anatomy of the heart in which the internal jugular
referred to as a plume.24 Placoid diseases such as acute posterior vein directly empties into the superior vena cava only on the
multifocal placoid pigment epitheliopathy and disorders such as right side, perhaps explaining the development of venous pres-
laser maculopathy have been characterised on OCT by hyper-­ sure complications on this side. In our other unilateral cases,
reflective lesions extending into the HFL.25–29 The HFL may act however, we did not note a predilection for right eye disease.
as a conduit or conducting track for various materials due to its The third factor associated with HFL haemorrhage in our
smooth, continuous and densely packed linear axonal structure series was likely independent of the vulnerabilities of the DCP
that is lacking in tight junctions, synapses, barriers or interrup- and more related to subretinal bleeding from the choroidal
tions to flow. vasculature, with subsequent tracking of the haemorrhage into
The advent of OCTA has elucidated the organisation of the HFL. Kim and colleagues38 described deep radiating intraretinal
retinal vasculature, which comprised four distinct plexuses: haemorrhage associated with small submacular haemorrhages in
the superficial, middle and deep capillary plexus, as well as the 19.4% of eyes with PCV and 7.5% of eyes with exudative age-­
radial peripapillary capillary plexus.6 30 Using OCTA imaging, related macular degeneration. We noted HFL haemorrhage in
the DCP has been localised between the outer 50% of the INL one case of PCV and in two cases of myopic degeneration in our
and the OPL.30 Recent studies have determined that the DCP is series, where the common feature was a thick subretinal haem-
the major level of venous outflow,10 11 and may be at greatest risk orrhage in the centre of the fovea which extended into the HFL
of injury and disruption secondary to acute changes in venous in the presence or absence of choroidal neovascularisation. PCV
pressure transmitted systemically or occurring locally. The (also known as aneurysmal type 1 neovascularisation) may be
proposed mechanism for HFL haemorrhage is analogous to that associated with increased haemorrhagic complications caused by
of formation of exudate around the macula in a star shape: blood abnormal haemodynamic forces leading to an increased propen-
from the DCP diffusing posteriorly to track along the densely sity for blood to track in HFL.39 40
compacted HFL, which can act as a conduit for blood, lipid and Bilateral deep retinal haemorrhages have been previously
other materials. This study has identified three factors (table 2) noted in Terson’s syndrome, Valsalva retinopathy and whip-
integral to the pathogenesis of HFL haemorrhage: (1) disorders lash retinopathy.8 41 42 However, these papers did not focus on
affecting systemic central venous pressure (ie, increased intra- the distinctive OCT and clinical features of radial, petaloid or
cranial pressure secondary to Terson’s syndrome or complica- feathery deep, intraretinal blood as identified in our series, nor
tions due to anaesthesia) secondarily affecting the retinal veins; were there details about the source of the blood from the DCP
(2) irregularities in retinal venous pressure due local retinovas- with extension into the HFL. Idiopathic unilateral deep retinal
cular causes (ie, retinal vein occlusion, Mac Tel type 2); and (3) haemorrhages were described by Gass43 in 1997 and subse-
pressure-­independent local choroidal vascular disorders. quently in a series of 11 eyes, but inciting causes and systemic
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14
findings were not identified and the association with HFL and Retina Department, Vitreous Retina Macula Consultants of New York, New York,
venous abnormalities (local and systemic) affecting the DCP New York, USA
was not realised.44 Haemorrhagic cystoid macular oedema was
described prior to availability of OCT as intraretinal haemor- Funding This study was funded by Research to Prevent Blindness.
rhage within the cystoid spaces of macular oedema featuring Competing interests None declared.
intracystic layering of blood and a round shape: these features Patient consent for publication Not required.
are not analogous to the cases of haemorrhage in HFL in our Ethics approval Institutional Review Board approval was obtained by coauthors
series where cystoid macular oedema was not a prominent according to the guidelines of their respective institutions. This study adhered to the
feature.45 46 A bilateral haemorrhagic maculopathy has also been rules of the Health Insurance Portability and Accountability Act and followed the
described after subarachnoid and epidural injections and endo- tenets of the Declaration of Helsinki.
scopic spinal surgery as a result of bleeding from the DCP, but Provenance and peer review Not commissioned; externally peer reviewed.
again the characteristic pattern of haemorrhage due to radialisa- Data availability statement All data relevant to the study are included in the
tion in HFL was not noted.34 47–50 article or uploaded as supplementary information. Only deidentified data are used in
While a radial, petaloid and feathery pattern of haemorrhage table 1. The OCT and retina deidentified images are available upon request from the
contributing author.
was the predominant finding in all of our cases of increased
systemic central venous pressure, as in Terson’s syndrome, inner ORCID iDs
retinal or preretinal haemorrhage was also present in certain Caroline R Baumal http://​orcid.​org/​0000-​0002-​3651-​8210
cases. We postulate that with more severe or sustained increases Francesco Pichi http://​orcid.​org/​0000-​0002-​7357-​4166
Giuseppe Querques http://​orcid.​org/​0000-​0002-​3292-​9581
in retinal venous pressure, there will be a greater preponderance Andrea Govetto http://​orcid.​org/​0000-​0003-​2192-​810X
for inner retinal haemorrhage, originating from the superficial Alessandro Invernizzi http://​orcid.​org/​0000-​0003-​3400-​1987
retinal capillary plexus, in addition to the DCP. This may be a
parallel mechanism explaining the development of PAMM and References
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