REVIEW Non-mydriatic fundus photography: a practical ... · cannot give useful photographic images,...

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Non-mydriatic fundus photography: a practical review for the neurologist Devin D Mackay, 1 Beau B Bruce 2,3 1 Departments of Neurology, Ophthalmology, and Neurosurgery, Indiana University School of Medicine, Indianapolis, Indiana, USA 2 Departments of Ophthalmology and Neurology, Emory University School of Medicine, Atlanta, Georgia, USA 3 Department of Epidemiology, Rollins School of Public Health and Laney Graduate School, Emory University, Atlanta, Georgia, USA Correspondence to Dr Beau B Bruce, Departments of Ophthalmology and Neurology, Neuro- Ophthalmology Unit, Emory Eye Center, The Emory Clinic, Emory University School of Medicine, 1365-B Clifton Road NE, Atlanta, GA 30322, USA; [email protected] Accepted 14 June 2016 Published Online First 12 July 2016 To cite: Mackay DD, Bruce BB. Pract Neurol 2016;16:343351. ABSTRACT Declining proficiency in direct ophthalmoscopy by non-ophthalmologists has spurred a search for alternative methods of ocular fundus examination. Recent technological advances have improved the ease of use and quality of non- mydriatic fundus photography, increasing its suitability for clinical care. As the availability of this technology continues to improve, neurologists will need to be familiar with its advantages, limitations and potential applications in the clinical care of patients with neurological conditions. INTRODUCTION Examination of the ocular fundus fre- quently yields important information that influences the clinical care of patients with neurological disease. However, difficulty performing ophthalmoscopy has contribu- ted to the demise of ophthalmoscopy by non-ophthalmologists. 1 The technical bar- riers of using a direct ophthalmoscope have led to renewed interest in alternative methods of viewing the optic disc, retina and retinal vessels. Technical advances coupled with the continued relevance of the funduscopic examination have driven interest in non-mydriatic fundus photog- raphy. Although it has been used since the 1970s, the technology has only recently advanced to the point of quickly obtaining high-quality fundus photographs, with minimal operator training and to rival the quality of mydriatic fundus cameras. Furthermore, research over the past decade has clarified its potential role in clinical care. As neurologists are among the most prominent non-ophthalmologists to gather information from the ocular fundus exam- ination for use in clinical care, it is import- ant that they are familiar with non-mydriatic fundus photography, its practical use in clinical settings, and condi- tions that may be more easily diagnosed or managed with its use. HOW DOES NON-MYDRIATIC FUNDUS PHOTOGRAPHY WORK? A cooperative patient sits in front of the fundus camera in a room with ambient lighting minimised ( figure 1) or turned off. However, if the ambient lighting cannot be adjusted, the clinician may place an opaque cover supported by a frame over the front of the camera and over the patients head and shoulders. The patient looks forward into the camera at a fixation light, and infrared fundus videography is used to focus on the region of interest. Many non-mydriatic cameras have software that automatically detects the posterior pole of the eye and takes a photograph when the back of the eye is in focus. Light in the infrared spectrum does not stimulate pupillary contraction. However, an infrared light source alone cannot give useful photographic images, and a flash is still needed. Sensitive image sensors in digital non-mydriatic fundus cameras allow the use of low flash set- tings. This helps to limit the amount of persistent pupillary constriction following the first image obtained with a flash, although the best quality pictures are obtained after an interphotographic inter- val of 3060 s. 2 Advances in digital photography technology have paved the way for additional features that make non-mydriatic fundus cameras easier to use, including autofocusing and auto- alignment mechanisms, user interface software with task automation and the ability to print images, export them to a database or electronic medical record, or share them electronically using a network or internet connection. WHAT EVIDENCE SUPPORTS THE USE OF NON-MYDRIATIC FUNDUS PHOTOGRAPHY IN NON-OPHTHALMOLOGY SETTINGS? A growing body of research has evaluated the impact of non-mydriatic fundus REVIEW Mackay DD, Bruce BB. Pract Neurol 2016;16:343351. doi:10.1136/practneurol-2016-001443 343 on April 11, 2020 by guest. Protected by copyright. http://pn.bmj.com/ Pract Neurol: first published as 10.1136/practneurol-2016-001443 on 12 July 2016. Downloaded from

Transcript of REVIEW Non-mydriatic fundus photography: a practical ... · cannot give useful photographic images,...

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Non-mydriatic fundus photography:a practical review for the neurologist

Devin D Mackay,1 Beau B Bruce2,3

1Departments of Neurology,Ophthalmology, andNeurosurgery, Indiana UniversitySchool of Medicine, Indianapolis,Indiana, USA2Departments of Ophthalmologyand Neurology, Emory UniversitySchool of Medicine, Atlanta,Georgia, USA3Department of Epidemiology,Rollins School of Public Healthand Laney Graduate School,Emory University, Atlanta,Georgia, USA

Correspondence toDr Beau B Bruce, Departmentsof Ophthalmology andNeurology, Neuro-Ophthalmology Unit, Emory EyeCenter, The Emory Clinic, EmoryUniversity School of Medicine,1365-B Clifton Road NE,Atlanta, GA 30322, USA;[email protected]

Accepted 14 June 2016Published Online First12 July 2016

To cite: Mackay DD,Bruce BB. Pract Neurol2016;16:343–351.

ABSTRACTDeclining proficiency in direct ophthalmoscopyby non-ophthalmologists has spurred a searchfor alternative methods of ocular fundusexamination. Recent technological advances haveimproved the ease of use and quality of non-mydriatic fundus photography, increasing itssuitability for clinical care. As the availability ofthis technology continues to improve,neurologists will need to be familiar with itsadvantages, limitations and potential applicationsin the clinical care of patients with neurologicalconditions.

INTRODUCTIONExamination of the ocular fundus fre-quently yields important information thatinfluences the clinical care of patients withneurological disease. However, difficultyperforming ophthalmoscopy has contribu-ted to the demise of ophthalmoscopy bynon-ophthalmologists.1 The technical bar-riers of using a direct ophthalmoscopehave led to renewed interest in alternativemethods of viewing the optic disc, retinaand retinal vessels. Technical advancescoupled with the continued relevance ofthe funduscopic examination have driveninterest in non-mydriatic fundus photog-raphy. Although it has been used since the1970s, the technology has only recentlyadvanced to the point of quickly obtaininghigh-quality fundus photographs, withminimal operator training and to rival thequality of mydriatic fundus cameras.Furthermore, research over the past decadehas clarified its potential role in clinicalcare. As neurologists are among the mostprominent non-ophthalmologists to gatherinformation from the ocular fundus exam-ination for use in clinical care, it is import-ant that they are familiar withnon-mydriatic fundus photography, itspractical use in clinical settings, and condi-tions that may be more easily diagnosed ormanaged with its use.

HOW DOES NON-MYDRIATICFUNDUS PHOTOGRAPHY WORK?A cooperative patient sits in front of thefundus camera in a room with ambientlighting minimised (figure 1) or turnedoff. However, if the ambient lightingcannot be adjusted, the clinician mayplace an opaque cover supported by aframe over the front of the camera andover the patient’s head and shoulders.The patient looks forward into the cameraat a fixation light, and infrared fundusvideography is used to focus on the regionof interest. Many non-mydriatic camerashave software that automatically detectsthe posterior pole of the eye and takes aphotograph when the back of the eye is infocus. Light in the infrared spectrum doesnot stimulate pupillary contraction.However, an infrared light source alonecannot give useful photographic images,and a flash is still needed. Sensitive imagesensors in digital non-mydriatic funduscameras allow the use of low flash set-tings. This helps to limit the amount ofpersistent pupillary constriction followingthe first image obtained with a flash,although the best quality pictures areobtained after an interphotographic inter-val of 30–60 s.2 Advances in digitalphotography technology have paved theway for additional features that makenon-mydriatic fundus cameras easier touse, including autofocusing and auto-alignment mechanisms, user interfacesoftware with task automation and theability to print images, export them to adatabase or electronic medical record, orshare them electronically using a networkor internet connection.

WHAT EVIDENCE SUPPORTS THE USEOF NON-MYDRIATIC FUNDUSPHOTOGRAPHY INNON-OPHTHALMOLOGY SETTINGS?A growing body of research has evaluatedthe impact of non-mydriatic fundus

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photography in the emergency department. A cohortof 350 adult patients was enrolled in the FundusPhotography versus Ophthalmoscopy Trial Outcomesin the Emergency Department (FOTO-ED) study.Inclusion criteria included a chief complaint of head-ache, acute focal neurological deficit, acute visionchange or a diastolic blood pressure of at least120 mm Hg. Forty-four of the 350 patients (13%)had a relevant ocular finding on fundus photography(optic disc oedema, intraocular haemorrhage, severehypertensive retinopathy, arterial vascular occlusion oroptic disc pallor). Eleven of the 44 findings wereknown before the patients presented to the emergencydepartment; of the remaining 33 findings, 6 werefound during ophthalmology consultation and theother 27 were identified only by fundus photography.Only 5 of the 33 patients with relevant ocular find-ings that were not known before presentation under-went a funduscopic examination by an emergencyphysician, all of which were documented as normal.3

Phase I of the FOTO-ED study focused on the feasi-bility of non-mydriatic fundus photography in theemergency department and found that 83% of the350 patients had a least one eye with a high-qualityphotograph. Nurse practitioners were given brieftraining and took the photographs used in the study,with a median image acquisition time of 1.9 min persession. Ease and speed of image acquisition wererated highly by the nurse practitioners and patients.4

Phase II of the FOTO-ED study focused on diagnos-tic accuracy and use of non-mydriatic fundus photog-raphy in the emergency department.5 In this phase,emergency physicians were given access to the photo-graphs taken during the visit, and could use them tohelp influence patient care. Three hundred and fifty-four patients were enrolled and 35 (10%) were foundto have relevant findings on fundus photographs.Emergency department physicians reviewed thephotographs of 238 patients (68%), identified 16 of

the 35 relevant findings (46%) using the photographsand reported them to be helpful for 125 patients(35%).In a separate study of patients with headache pre-

senting to an academic emergency department, 8.5%(42/497) had abnormal ocular fundus findingsdetected via non-mydriatic fundus photography.Fourteen of the 41 patients (41%) with abnormalfundus findings who underwent MRI had normalimaging.6

In an Australian population, 693 patients with tran-sient ischaemic attacks and acute stroke underwentpharmacological pupillary dilation and fundus pho-tography for assessment of retinal microvascular signs(retinopathy, focal arteriolar narrowing, arteriovenousnicking and an enhanced arteriolar light reflex). Allretinal microvascular signs were more prevalent inpatients with transient ischaemic attacks or strokethan in control subjects, suggesting that fundus pho-tography may provide useful information in the riskstratification of patients with suspected cerebrovascu-lar disease.7

WHAT ARE POTENTIAL APPLICATIONS FORNON-MYDRIATIC FUNDUS PHOTOGRAPHY INNEUROLOGY?It is often difficult to discern the details of the opticdisc and other parts of the ocular fundus throughundilated pupils. The main hurdle is the technical dif-ficulty of using the ophthalmoscope. When this tech-nical barrier is removed, neurologists, even withoutspecific additional training, can use the ocular fundusexamination more easily to make informed decisionsregarding a patient’s care.Fundus photography in patients with uncontrolled

hypertension, headache, vision complaints or suspicionof cerebrovascular disease may give important informa-tion that influences patient management. Subtle andsometimes even not-so-subtle fundus abnormalities

Figure 1 Typical configuration of non-mydriatic fundus camera. The patient is seated in a chair opposite the fundus camera.A computer is attached to the device, and runs software that automates portions of the image acquisition process and allowsfor digital image review, storage and distribution.

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may be missed with a cursory funduscopic examinationin an outpatient clinic. For example, finding even mildoptic disc oedema should prompt an urgent workup toexclude serious underlying causes of elevated intracra-nial pressure (eg, cerebral venous thrombosis, tumour,obstructive hydrocephalus) in a patient whose head-ache may have otherwise been misdiagnosed asprimary. Finding optic disc pallor in a patient withunexplained neurological symptoms may suggestdemyelinating disease or its mimics. It could also alertthe clinician to obtain orbital MRI as well as brainimaging to exclude an orbital mass (eg, an optic nervesheath meningioma). A patient who presents to clinicfor stroke follow-up care with a blood pressure of 220/110 mm Hg and is found to have optic disc oedemawith retinal haemorrhages and exudates consistent withhypertensive retinopathy may prompt referral to theemergency department as a hypertensive emergency.Fundus photography has also been used in patients

with chronic neurological conditions, such as cerebro-vascular disease and dementia. The brain and retinaare similar in their embryological origin and physio-logical properties; this has inspired research intodirect visualisation of small vessels of the retina as asurrogate for intracranial small vessels, which cannotbe readily seen in vivo. The retinal vasculature can beseen non-invasively using fundus photography.Indeed, studies have shown a link between retinal vas-cular changes seen with fundus photography andstroke and dementia.8

Medical educationAcademic medical centres are uniquely positioned tobenefit from the acquisition of a non-mydriatic funduscamera, as the benefits may be more easily realised in alarge provider group in collaboration with other clini-cians and in the training of the next generation ofmedical professionals. Most medical students alsoreport that they prefer to use fundus photographs overdirect ophthalmoscopy, and 20% of students in onestudy reported that their primary reason for not per-forming an ocular fundus examination during a patientevaluation was discouragement by their preceptor.9 10

A photograph allows clinicians to evaluate the ocularfundus more easily, to emphasise the importance of theocular fundus examination in the complete evaluationof many classes of neurological disease, and to pointout key features of the ocular fundus to trainees in thecontext of an actual patient’s evaluation. It is easy toshare challenging cases or findings with other cliniciansand to facilitate the diagnostic evaluation.11 Usingfundus photography in medical education has thepotential to restore enthusiasm for the ocular fundusexamination in future generations of clinicians.

TelemedicineThe rise of telecommunications technology has intro-duced important telemedicine opportunities,

including ocular fundus photography interpretation.12

The use of telemedicine in acute stroke has increaseddramatically in recent years, despite significant regula-tory and other barriers to its implementation. Thesuccess of ‘telestroke’ evaluations has built upon rapidaccess to a specialist in areas where the specialist isnot readily physically available. Rapid fundus photo-graph interpretation through a teleophthalmologyconsultation may become standardised in the future.In the meantime, fundus photographs may be sharedwith other clinicians and colleagues electronically tohelp facilitate triage decisions.

ABNORMALITIES OF THE OCULAR FUNDUSREQUIRING URGENT EVALUATIONAll patients presenting to a neurologist with a visualcomplaint should be seen by an eye care specialist assoon as possible. Furthermore, the neurologist is likelyto encounter the following ocular fundus abnormal-ities relatively frequently, all of which generally indi-cate the need of an emergent or expedited workup.

Optic disc oedemaOptic disc oedema can be difficult to see with a directophthalmoscope in some patients; a fundus photo-graph may help. A fundus photograph may not clarifywhether a patient has very subtle optic disc oedema,but can help to look for other funduscopic signs ofoptic disc oedema. These signs include blurring of theoptic disc edges, filling in of the optic cup, peripapil-lary folds, obscuration of vessels as they cross theoptic disc margin, peripapillary retinal haemorrhages,optic nerve head hyperaemia and venous congestion(figure 2).13 Photographs can also be very useful indistinguishing pseudopapilloedema from true opticdisc oedema. For example, multifocal, irregular glo-bules (sometimes described as tapioca-like) within theoptic nerve head are diagnostic for optic nerve headdrusen (figure 3).

Optic disc pallorA normal optic disc is typically pink/orange in colour.An abnormally white optic disc appearance is referredto as optic disc pallor: a sign of damage to the opticnerve that takes at least 4–6 weeks to develop after aninjury. The pallor may be subtle, and also assessmentof optic disc colour is subjective and can be influencedby photographic exposure, adding to the difficulty indetecting optic disc pallor. In unilateral cases, it maybe easier to detect pallor by comparing fundus photo-graphs between the two eyes (figure 4). Details of thepallor may also help, such as definite pallor limited tothe superior or inferior portion of the optic disc, as inpatients with non-arteritic anterior ischaemic opticneuropathy. Optic disc pallor can provide additionalevidence for optic neuritis in a patient with suspecteddemyelinating disease. Moderate-to-severe generalisedpallor is accompanied by a noticeable lack of small

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vessels on the temporal part of the optic disc. Thus,abnormal optic disc colour is not the only abnormal-ity to suggest optic disc pallor.

Central or branch retinal artery occlusionPatients with central retinal artery occlusion classicallyexhibit a macular cherry-red spot with an otherwisepale retina, as the clinician sees the intact choroidalblood supply though the central (thinnest) part of themacula (figure 5). There may also be interruptions ofthe blood column within the retinal arteries giving theappearance of train cars, so-called ‘box-carring’. In 4–6 weeks, the retinal whitening resolves and the opticdisc may appear pale with attenuation of the retinalarterioles. An acute branch retinal artery occlusioncauses whitening of the portion of retina suppliedonly by the affected vessel. As in a central retinalartery occlusion, the whitening may only last severalweeks and the only clue may be attenuated arterioleswithin the affected area. Counterintuitively, it may bedifficult to detect widespread abnormalities such asthe retinal whitening from a central retinal arteryocclusion with a direct ophthalmoscope because thenarrow field of view makes it difficult to compareaffected and unaffected parts of the retina.

Central or branch retinal vein occlusionCentral retinal vein occlusion is typically asso-ciated with extensive flame-shaped haemorrhages

throughout the ocular fundus, dilated and tortuousretinal veins and there may be optic disc oedema.Branch retinal vein occlusion gives the same signsrestricted to the vascular drainage territory of theaffected vein branch (figure 6, occlusion at doublearrow). Branch occlusions typically occur at arterioven-ous crossings, as in this case (box 1). Risk factorsinclude increasing age, hypertension, diabetes mellitus,hyperlipidaemia, cigarette smoking andthrombophilia.14

Severe hypertensive retinopathyIt may be easier to see features of both mild andsevere hypertensive retinopathy with fundus photog-raphy than with direct ophthalmoscopy. Hypertensiveretinopathy is usually mild and is characterised byarteriolar narrowing as one of the earliest signs. Opticdisc oedema occurs in very severe hypertensive retin-opathy, and can usually be differentiated from othercauses of optic disc oedema by the presence of retinalhaemorrhages distant from the optic disc and exudatesthat indicate breakdown of the blood–retina barrier.Cotton wool spots (areas of retinal infarction) mayalso develop in severe cases.

Intraretinal haemorrhagesIntraretinal haemorrhages are a sign of blood vesseldamage, most often from hypertension, but their sig-nificance is not completely clear. A trial of 497 patientspresenting to a tertiary care academic emergencydepartment with headache found that 42 had ocularfundus abnormalities, 15 of which were isolated retinalhaemorrhages, presumably related to hypertension.Another 6 had grade III/IV hypertensive retinopathy,suggesting that half of the patients (21/42) with abnor-mal ocular fundus findings in this headache populationhad findings related to hypertension.

INTERPRETATION OF FUNDUS PHOTOGRAPHS BYNEUROLOGISTSNon-ophthalmologists are likely to interpret ocularfundus abnormalities more easily using photographsthan with direct ophthalmoscopy. Nevertheless,instruction in the approach to the ocular fundusexamination via photographs may help neurologists touse fundus photography in clinical care. While thereis no one universally advocated approach, having asystematic and organised approach to the examinationof the ocular fundus in a photograph has the potentialto improve the accuracy of interpretation.Nevertheless, it cannot be overemphasised that anophthalmologist must also evaluate all patients withvision loss, regardless of ocular fundus findings.As with any other diagnostic test, it is best to inter-

pret fundus photographs in the context of the clinicalhistory and examination findings. Such context isoften essential to know what findings may be inciden-tal or inconsequential, and what others may

Figure 2 Papilloedema in a patient with idiopathic intracranialhypertension. This photograph shows several key findings that,in combination, are quite specific for true optic disc oedema,including peripapillary retinal folds (concentric arcs identified bydashed arrows), partial optic disc vessel obscuration (doublearrow) and a small focal haemorrhage (arrow).

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contribute valuable information to the patient’s evalu-ation and inform further management decisions.15

As a generic approach to the ocular fundus examin-ation in a photograph, one may arbitrarily divide theocular fundus into regions: this prompts the clinicianto look for specific findings in each region.Determining which eye you are viewing can be facili-tated by remembering that the optic disc is closest tothe nose. Therefore, in a properly centred photographin which you see the macula and the optic disc, youwill find the optic disc to the left side of the photo-graph in the left eye and to the right side in the righteye.

Optic discKey features of the optic disc to be evaluated during afundus examination include the disc colour, sharpnessof margins and the cup-to-disc ratio. In a photograph,the cup-to-disc ratio can be obvious, or difficult todiscern, depending on the patient. An enlargedcup-to-disc ratio may be normal and physiological, or

associated with glaucoma. The temporal portion ofthe optic disc is normally slightly more pale than thenasal portion, but excessive or generalised optic discpallor can suggest optic neuropathy (figure 4). In thesetting of a relative afferent pupillary defect, unilateralor asymmetrical optic disc pallor confirms damage tothe optic nerve that began at least 4–6 weeks before.Blurring of the optic disc margins is a sign of opticdisc oedema, and the differential diagnosis is influ-enced by whether the oedema is segmental or general-ised, and unilateral or bilateral.

MaculaThe macula is normally found temporal and slightlyinferior to the optic disc and contains densely packedcone photoreceptors that are essential for high-acuitycolour central vision. The foveal light reflex is anormal reflection of light from the thin retinal layersat the fovea and can sometimes be seen in fundusphotographs. A decreased foveal light reflex in oneeye associated with a decrease in visual acuity in that

Figure 3 Prominent optic nerve head drusen. There are irregular, tapioca-like globules in this patient’s optic nerve heads: right eye(A) and left eye (B). Less obvious examples require careful examination of the optic nerve head to screen for this not uncommonmimic of optic disc oedema.

Figure 4 Unilateral optic disc pallor. The right optic disc (A) is normal in colour. The left optic disc (B) exhibits subtle pallor,particularly temporally (right side of the disc in the photograph). Comparing the optic discs from each eye in photographs is avaluable tool in the detection of unilateral optic disc pallor.

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eye can indicate a foveal abnormality, such as macularoedema. Neuroretinitis, caused by inflammation ofthe retina and optic disc, is primarily recognised by anassociated macular-star pattern of exudates, often withoptic disc oedema (figure 7). Other macular abnor-malities such as haemorrhage are generally moreeasily seen with fundus photographs than via directophthalmoscopy.

Retinal vesselsDilated retinal vessels may develop in papilloedema orin occlusive disorders of the retinal veins, such as acentral or branch retinal vein occlusion. Arteriovenousnicking may occur in patients with chronic hyperten-sion, in which a hard atherosclerotic arteriole

compresses a retinal vein, resulting in a focal changein the contour of the vein and a ‘nicked’ appearance(figure 6, arrows). Patients with a history of transientmonocular vision disturbance should be examined fora Hollenhorst plaque, which is a sign of cholesterolembolisation from a proximal atherosclerotic source(figure 8).

Mid-peripheral retinaRetinal abnormalities such as haemorrhages, exudatesand microaneurysms are often difficult to detect witha direct ophthalmoscope and may be more easilydetected in a fundus photograph. Haemorrhages andexudates distant from the optic disc can occur in

Figure 5 Central retinal artery occlusion. Note the macularcherry red spot (arrow) with an otherwise pale retina, as theclinician can see the intact choroidal blood supply though thecentral (thinnest) part of the macula.

Figure 6 Branch retinal vein occlusion (BRVO). Note thepresence of haemorrhages, cotton wool spots and tortuous anddilated veins distal to the site of BRVO (double arrow) involvingthe superotemporal macula. Arteriovenous nicking is also seenas a result of uncontrolled systemic hypertension (arrows).

Box 1 Case study

A 40-year-old woman presented for evaluation of prob-able idiopathic intracranial hypertension (IIH). She has ahistory of refractory hypertension and headaches. Shehad several months of episodic vision disturbances withlightheadedness and worsening of headaches. An MRI ofthe brain showed an empty sella turcica. A neurologistdiagnosed IIH, without a lumbar puncture at that time.Several months later, she noticed a dark spot in thevision of her right eye. Her neurologist then arranged fora lumbar puncture, which showed an opening pressureof 22 cm of water with normal cerebrospinal fluid. Theneurologist documented ‘mild blurring of the diskmargins’ and started her on acetazolamide for a pre-sumed vision disturbance related to IIH.On examination, her body mass index was 43.1 kg/m2

and blood pressure was initially 216/143 mm Hg. Visualacuity was 6/60 in the right eye and 6/6 in the left eye.There was no relative afferent pupillary defect.Confrontation visual fields showed decreased vision infer-onasally in the right eye and were full in the left eye.Fundus photographs showed pink, sharp optic discs

with no disc oedema, but the right eye retina showedextensive retinal haemorrhages localised to the supero-temporal macula with scattered flame-shaped haemor-rhages and cotton wool spots in the same localised area,in a pattern consistent with a branch retinal vein occlu-sion (figure 6).IIH had been misdiagnosed in this case, partially

because of difficulty performing funduscopy. It was pre-sumed that her vision disturbance was from IIH, althougha fundus photograph clearly showed significant retinalabnormalities without optic disc oedema that would havebeen easily discerned by a non-ophthalmologist assistedby a photograph. A fundus photograph performed by thereferring neurologist would have localised the abnormal-ity, which was not consistent with IIH, prevented unneces-sary invasive testing, and facilitated referral to anophthalmologist for evaluation and management.

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conditions such as hypertensive retinopathy and dia-betic retinopathy and would not be expected in otherconditions, such as papilloedema from raised intracra-nial pressure. Microaneurysms appear as small dots ofblood in the retina due to outpouching of retinalcapillaries, and can occur in diabetic retinopathy.

Other normal findingsA highly reflective layer, sometimes surrounding theoptic nerve and macula, may be visible in photographsin younger patients. This is the inner limiting

membrane, and is a normal finding that may confusesome non-ophthalmologists. Patients with lightly pig-mented skin can have a distinctive ocular fundusappearance with ‘tangles’ of orange streaks behind theretinal vessels, which are the choroidal vessels, and area normal finding called a ‘blonde’ fundus. Conversely,patients with more darkly pigmented skin tend tohave a more ‘tigroid’ appearance that resembles tigerstripes, which represents the choroidal vessels againsta background of darker pigments, which is also anormal finding.

ArtefactsArtefacts are common in fundus photography andmay result from incorrect patient–camera orientation,excessively small pupils, camera lens debris or othercauses. A faded whitish area with a gradient from theedge of the photograph may be a sign of artefact fromthe pupil border in patients with smaller pupils. Theremay be other cloudy artefacts, confirmed as artefac-tual by comparing with photographs from the sameeye in a slightly different position (in which the arte-fact appears in a slightly different location), or fromthe contralateral eye.

WHAT ARE ADVANTAGES AND DISADVANTAGESOF NON-MYDRIATIC FUNDUS PHOTOGRAPHY INNEUROLOGY?StrengthsAs with any diagnostic tool, an accurate understand-ing of the strengths and limitations of non-mydriaticfundus photography can help clinicians to knowwhen fundus photographs may be useful. A majoradvantage is convenience. Obtaining images from afundus camera in the emergency department or anoutpatient clinic is relatively fast and easy, with themedian time of image acquisition in phase I of theFOTO-ED study being just 1.9 min.4 As handheldnon-mydriatic fundus camera technology improvesand becomes more commonplace, it should help oneto obtain a view of the ocular fundus while avoidingpharmacological pupil dilatation in critical carepatients with intracranial pathology in whom follow-ing a pupillary examination can be clinically valuable.Clinicians and students also find fundus photographinterpretation easier than using a direct ophthalmo-scope through an undilated pupil.5 9 10 The qualityof the images is also very good in most patients,rivalling the quality of mydriatic fundus cameras.The resolution of the images typically also allows fordigital zoom to appreciate finer details of the ocularfundus. As was also shown in phase I of theFOTO-ED study, nurse practitioners who operatedthe fundus camera required minimal training. Theimages are also available to share with others foreducational purposes, to facilitate triage decisionsand to enhance medical education.11 16 The photo-graphs may also serve as a form of documentation,

Figure 7 Neuroretinitis. This photograph depicts optic discpallor for optic nerve damage as well as yellowish exudates inthe peripapillary retina and macula that are radially oriented in a‘star’ pattern, consistent with neuroretinitis. Optic disc oedemamay be the first sign, followed days to weeks later by retinalexudates suggestive of retinal inflammation.

Figure 8 Hollenhorst plaque. There is a cholesterol embolism(Hollenhorst plaque, arrow) in a superior retinal arteriole, whichcame from a proximal atherosclerotic source.

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which may help in future clinic visits and medicole-gal cases. For the purposes of a neurology evaluation,non-mydriatic fundus photography allows for adetailed assessment of the ocular fundus, withoutpupillary dilatation.

LimitationsOne disadvantage or limitation of non-mydriaticfundus photography is the cost of equipment, whichcan be around £17 000–£22 000 ($25 000–$30 000)depending on the model. However, prices are likelyto fall with more widespread adoption of the technol-ogy. Also, current non-mydriatic cameras require apatient to be alert and cooperative, to sit still and tobe able to follow simple commands, which applies tomost outpatients, but not all. There are several modelsof handheld non-mydriatic cameras that may be usefulfor uncooperative patients in acute care settings, suchas the intensive care unit, although the quality ofimages is currently inferior to stationary desktopmodels and the devices are considerably more difficultto use. Devices that attach to smartphones to allowfundus photographs to be taken have become morepopular in recent years, but they generally still requirepupillary dilatation for adequate views of the ocularfundus, which limits their use among neurologists.Non-mydriatic fundus photographs also do notprovide a dynamic view of the ocular fundus,meaning that the evaluation of spontaneous venouspulsations, subtle abnormalities of visual fixation suchas low amplitude nystagmus, or the rare occurrence oftracking a moving retinal embolus remain reserved fora live funduscopic view via an ophthalmoscope or theoccasional camera with video capabilities.

CONCLUSIONThe ocular fundus examination is still important,despite the demise of direct ophthalmoscopy in recent

decades. The non-mydriatic fundus camera is an alter-native tool that bypasses the technical difficulty of thedirect ophthalmoscope and makes the ocular fundusexamination more accessible. A combination of clin-ician discomfort with the use of a direct ophthalmo-scope, persistent relevance of the ocular fundusexamination and increasing availability of non-mydriatic fundus cameras in clinical care is creatingmomentum for more widespread adoption of this tech-nology. Neurologists are poised to benefit from thismomentum and should be familiar with the applicationof non-mydriatic fundus photography in clinical care.

Contributors All authors contributed to the writing and finalapproval of this manuscript.

Funding Research to Prevent Blindness, National Institute ofNeurological Disorders and Stroke (R01-NS089694), NationalEye Institute (P30-EY006360).

Competing interests None declared.

Provenance and peer review Commissioned; externally peerreviewed. This paper was reviewed by Christian Lueck,Canberra, Australia.

REFERENCES1 Mackay DD, Garza PS, Bruce BB, et al. The demise of direct

ophthalmoscopy: a modern clinical challenge. Neurol ClinPract 2015;5:150–7.

2 Lamirel C, Bruce BB, Wright DW, et al. Quality ofnonmydriatic digital fundus photography obtained by nursepractitioners in the emergency department: the FOTO-EDstudy. Ophthalmology 2012;119:617–24.

3 Bruce BB, Lamirel C, Wright DW, et al. Nonmydriatic ocularfundus photography in the emergency department. N Engl JMed 2011;364:387–9.

4 Bruce BB, Lamirel C, Biousse V, et al. Feasibility ofnonmydriatic ocular fundus photography in the emergencydepartment: phase I of the FOTO-ED study. Acad Emerg Med2011;18:928–33.

5 Bruce BB, Thulasi P, Fraser CL, et al. Diagnostic accuracy anduse of nonmydriatic ocular fundus photography by emergencyphysicians: phase II of the FOTO-ED study. Ann Emerg Med2013;62:28–33.

6 Thulasi P, Fraser CL, Biousse V, et al. Nonmydriatic ocularfundus photography among headache patients in an emergencydepartment. Neurology 2013;80:432–7.

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Key points

▸ Non-mydriatic fundus photography is an effectivealternative to direct ophthalmoscopy for examiningthe ocular fundus in non-ophthalmology settings.

▸ Even without additional training, it is easier to detectand interpret abnormalities of the ocular fundus withphotographs rather than with direct ophthalmoscopy.

▸ With increasing availability of non-mydriatic fundusphotography, neurologists need to become familiarwith its advantages and limitations in clinical care.

▸ Rapidly advancing technology is improving both thequality and availability of non-mydriatic fundusphotography.

▸ Fundus photography has the potential to improvemedical education about the ocular fundus examination.

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16 Bidot S, Bruce BB, Newman NJ, et al. Nonmydriatic retinalphotography in the evaluation of acute neurologic conditions.Neurol Clin Pract 2013;3:527–31.

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