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Abstract
A boy in his mid-teens presented with progressively increasing bleeding from the right eye and nostril intermittently over a period of 6 weeks. A complete ophthalmic examination revealed nothing significant. His otorhinological examination and haematological investigations were within normal limits. The patient came a month later with frank bleeding from the right eye. Ophthalmic examination revealed hyperaemia and maceration of the right lower palpebral conjunctiva. A histopathological examination of conjunctival scrapings from the site showed abnormal dilated blood vessels suggestive of a vascular malformation. Digital subtraction angiography confirmed the presence of a conjunctival micro arteriovenous malformation supplied by the external carotid and ophthalmic artery branches. He underwent successful transarterial Onyx embolisation resulting in complete resolution of the haemolacria.
- Ophthalmology
- Interventional radiology
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Background
Haemolacria or ‘bloody tears’ is an alarming ophthalmic condition characterised by the presence of blood in tears. Though an uncommon presentation, some previously reported causes include conjunctival infective/inflammatory conditions, malignancies, trauma, orbital varices, adnexal haemangiomas, blood dyscrasias or anticoagulant use, retrograde epistaxis, vicarious menstruation (cyclical bleeding from extrauterine organs such as the eyelids, conjunctiva, ear, nose or skin during menstruation), Valsalva manoeuvre and factitious disorders due to hysteria/psychiatric illness.1–6 This is the first reported case of haemolacria due to an underlying conjunctival micro arteriovenous malformation (AVM).
Case presentation
A boy in his early adolescence presented with painless intermittent progressively increasing spontaneous bleeding from his right eye and right nostril for 2 weeks. There was no history of recent trauma, bleeding from any other mucosal surfaces or psychiatric illness. He had undergone surgery for total anomalous pulmonary venous circulation (TAPVC) in early childhood. On examination, there was no active bleeding. His vision in both eyes was 6/6, and his anterior and posterior segments were within normal limits. Lacrimal sac syringing test was freely patent in both eyes, from both puncta, with no appearance of haemorrhage. An otorhinological consult along with MRI of the paranasal sinuses and orbit was normal. The patient returned a month later with recurrent haemolacria (figure 1A), which was aggravated by micturition. On examination there was no active bleed but there was maceration and haemorrhage evident in the hyperaemic lower forniceal conjunctiva (figure 1B). The bulbar conjunctiva, remainder of the anterior and posterior segments were within normal limits. Repeat lacrimal sac syringing of both puncta was freely patent in both eyes. The patient was asked to pass urine and frank bleeding was noted from the right eye post micturition (figure 1C). Histopathological examination of a scraping of the coagulum and forniceal conjunctiva revealed malformed blood vessels consistent with a vascular malformation (figure 1D). MRI with contrast and angiography of the orbit and paranasal sinuses however failed to reveal any gross macrovascular malformation. Re-evaluation by an otorhinolaryngologist excluded retrograde epistaxis. Cardiac evaluation by his prior treating cardiothoracic surgeon revealed stable postoperative changes with no new findings. The patient was then referred to an interventional neuroradiologist for further evaluation.
Clinical photographs. (A) External photograph provided by the patient during an episode of active bleed. (B) Photograph in the clinic shows pooling of blood in the inferior fornix. (C) Macrophotography shows conjunctival hyperaemia and maceration (black arrow) in the inferior conjunctival fornix. (D) Histopathology of scrapings from this site shows abnormal vascular channels (white arrow), dilated malformed blood vessels (black arrow) and a phlebolith (yellow arrow).
Investigations
All the relevant blood investigations were within normal limits including hemogram, prothrombin time/international normalised ratio (11.1 s/0.98), partial thromboplastin time (31 s) and a normocytic normochromic peripheral blood smear. He underwent diagnostic digital subtraction angiography (DSA). A prominent vascular ‘blush’ suggestive of a vascular nidus was seen at the inferotemporal aspect of the right orbit. The nidus was fed by two feeders from both the external and internal carotid vasculature—a medial palpebral branch of the ipsilateral ophthalmic artery (figure 2A, online supplemental video 1) and a lateral palpebral branch from the zygomatic branch of the ipsilateral internal maxillary artery (figure 2B, online supplemental video 2). A 3D rotational cone beam CT angiography confirmed the location of this vascular blush as corresponding to the site of bleeding from the inferior forniceal conjunctiva (figure 2C, online supplemental video 3). The findings were consistent with a conjunctival micro AVM.
Supplementary video
Supplementary video
Supplementary video
Digital subtraction angiography images. (A) Right internal carotid angiogram (lateral view) shows the medial palpebral branch of the supratrochlear artery, which itself originates from the ophthalmic artery. (B) Right external carotid angiogram (lateral view) shows the zygomatic branch of the internal maxillary artery supplying the conjunctival arteriovenous malformation (AVM). (C) 3D rotational cone beam CT angiography (frontal view) from the right internal maxillary artery shows the location of the conjunctival micro AVM along the inferior fornix.
Treatment
Unlike for clinically evident vascular malformations of the conjunctiva, surgical debulking and ocular surface reconstruction were not an option as the lesion was detected only on DSA. Hence, the patient was offered endovascular transarterial liquid embolisation via the external carotid (internal maxillary) artery. The procedure was performed via a transfemoral approach under general anaesthesia. Through a 5F Envoy guide catheter (Codman Neuro, USA) in the right internal maxillary artery, a 1.2F Marathon microcatheter (Medtronic, USA) over a 0.014′ Traxcess microwire (Microvention Terumo, USA) was navigated into the zygomatic branch to achieve a tip position as close to the feeding lateral palpebral branch as possible (figure 3A,B). There were prominent draining veins into the angular and retromandibular veins (figure 3C). Under serial negative roadmap guidance, 0.4 mL of Onyx-18 (Medtronic) was injected until complete filling of the AVM nidus was seen (figure 3D). Pauses in the injection were done whenever reflux into the medial palpebral branch was seen. Final check angiography from both external (figure 3E) and internal carotid arteries (figure 3F) revealed complete obliteration of the AVM nidus. The microcatheter was uneventfully retrieved.
Embolisation procedure. (A) Lateral view of microcatheter navigation into the zygomatic branch of the internal maxillary artery. (B) Superselective microcatheter angiogram shows better delineation of the conjunctival micro arteriovenous malformation (AVM). (C) Frontal view shows prominent draining veins into the angular and retromandibular veins. (D) Fluoroscopic appearance of the Onyx cast conforming to the nidus. Check postembolisation angiograms from the (E) external and (F) internal carotid arteries shows complete obliteration of the micro AVM nidus.
Outcome and follow-up
Postprocedure, the black pigment of the Onyx cast was visible at the site of the conjunctival AVM (figure 4A). Apart from mild pain and eyelid oedema, the remainder of the postprocedure period was uneventful. At 2 weeks review, there had been no further episodes of haemolacria and the right lower fornix showed minimal scarring (figure 4B). He continues to remain asymptomatic at 6-month follow-up.
Treatment related clinical images. (A) Postembolisation appearance of black pigmented Onyx embolic agent. (B) Two-week postembolisation clinical photograph shows normalisation of the conjunctiva.
Discussion
Haemolacria, characterised by spontaneous bleeding from the ocular surface, is a rare condition. The degree of haemorrhage can range from sanguineous watery discharge to frank bleeding with a variety of causes previously reported.1–6 A meticulous history should include previous trauma, provoking and mitigating factors such as Valsalva manoeuvrers, variability with head position and synchronicity with menstruation,1 4 with an interesting provoking factor in our case being micturition. This could be related to reduced vascular tone secondary to parasympathetic activity, a mechanism similar to penile erection.7 Bleeding elsewhere in the body may suggest systemic conditions such as bleeding disorders, or vascular malformation syndromes such as hereditary haemorrhagic telangiectasia or endometriosis.1 8–11 Our case coincidentally had a previously surgically corrected TAPVC. TAPVC is a congenital cyanotic heart disease where the pulmonary veins drain abnormally into the right, rather than the left atrium and bleeding has not been reported in surgically corrected cases.12 Finally, functional disorders are seen predominantly in female teenagers and are a diagnosis of exclusion requiring psychiatric evaluation.6
Clinically, a detailed external examination in an attempt to anatomically localise the source of the bleeding to the conjunctiva, eyelid margins, lacrimal glands or the deeper orbit should be attempted by looking for abnormal vasculature, erosions/ulcerations, enlargements or tenderness.13 Paradoxical haemolacria via the lacrimal punctae can be seen with epistaxis and should include assessment of patency of the nasolacrimal duct and nasal cavity examination.14 Laboratory investigations should include a complete hemogram and coagulation profile. Radiological imaging, either MRI or CT with contrast of the orbit and paranasal sinuses is required to look for mass lesions that could represent vascular lesions or malignancies.
The diagnosis in our case was initially delayed by non-specific clinical examination findings and a normal MRI. Only a conjunctival biopsy and DSA confirmed the diagnosis of a conjunctival micro AVM. This highlights the utility of DSA in such cryptogenic cases where it is the gold standard for detection and analysis of vascular malformations. An important caveat however, is that DSA may be suboptimal in detecting vascular malformations without arteriovenous shunting such as venous malformations or telangiectasias. Shunting malformations such as AVMs are best evaluated by DSA and can be graded into low-flow or high-flow types based on the ISSVA (The International Society for the Study of Vascular Anomalies) classification. This allows for treatment planning.15
Endovascular treatment of soft tissue AVMs is mainly with the use of transarterial microcatheter techniques and embolisation using liquid agents. When feasible, a non-eloquent (ie, not supplying eloquent areas of brain or retina) external carotid branch is preferably cannulated, as in our case. Two main types of liquid embolic agents are used in neuroendovascular procedures—cyanoacrylate glue and ethyl-vinyl alcohol based polymers.16 Cyanoacrylate glue was not preferred in our case for several reasons.16 It has inherent tissue toxicity that could lead to exaggerated conjunctival irritation and necrosis. It also has rapid polymerisation times, requiring faster injection rates with consequent unpredictability of glue percolation. Further, inadvertent percolation of glue into the ophthalmic artery via intranidal ECA to ICA anastomosis could result in blindness. We preferred using the Onyx Liquid Embolic System (Medtronic) which is an EVOH based liquid embolic polymer. Unlike glue, it has a much slower polymerisation time allowing for a longer, more controlled injection rate.16 Further, it is non-adhesive and more inert and better tolerated by the adjoining soft tissue.
This is the first report of a case of conjunctival micro AVM resulting in haemolacria that was successfully treated by endovascular embolisation. A DSA is crucial in elucidating the underlying vascular anomaly in cryptogenic cases and interventional neuroradiological techniques are well suited to manage such cases. This rare cause of haemolacria should be considered when other common causes have been excluded.
Learning points
Haemolacria has a varied aetiology and has to be investigated thoroughly before labelling it secondary to hysteria or malingering.
Digital subtraction angiography is the gold standard for detection of underlying occult vascular malformations in cases of cryptogenic haemolacria.
Histopathological examination of clinically suspicious lesions may be diagnostic of micro arteriovenous malformations (AVMs) and is particularly useful when cross-sectional imaging is negative.
For soft tissue conjunctival AVMs, transarterial embolisation with ethyl-vinyl alcohol based liquid embolic agents is a feasible option.
Management of AVMs of the orbit and adnexa requires a multi-disciplinary approach involving the oculoplastic surgeon, pathologist and interventional neuroradiologist.
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Footnotes
Contributors AK, KRVJ, CN and CJ were responsible for drafting the text, sourcing and editing clinical images, investigation results, drawing original diagrams and algorithms, and critical revision for important intellectual content. AK, KRVJ, CN and CJ gave final approval of the manuscript.
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Case reports provide a valuable learning resource for the scientific community and can indicate areas of interest for future research. They should not be used in isolation to guide treatment choices or public health policy.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
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