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Biousse 2017

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Published Ahead of Print on December 22, 2017 as 10.1212/WNL.

0000000000004868
VIEWS & REVIEWS

Ophthalmoscopy in the 21st century


The 2017 H. Houston Merritt Lecture
Valérie Biousse, MD,* Beau B. Bruce, MD, PhD, and Nancy J. Newman, MD* Correspondence

®
Dr. Newman
Neurology 2018;90:1-9. doi:10.1212/WNL.0000000000004868 [email protected]

Abstract
Although the usefulness of viewing the ocular fundus is well-recognized, ophthalmoscopy is
infrequently and poorly performed by most nonophthalmologist physicians, including neu-
rologists. Barriers to the practice of ophthalmoscopy by nonophthalmologists include not only
the technical difficulty related to direct ophthalmoscopy, but also lack of adequate training and
discouragement by preceptors. Recent studies have shown that digital retinal fundus photo-
graphs with electronic transmission and remote interpretation of images by an ophthalmologist
are an efficient and reliable way to allow examination of the ocular fundus in patients with
systemic disorders such as diabetes mellitus. Ocular fundus photographs obtained without
pharmacologic dilation of the pupil using nonmydriatic fundus cameras could be of great value
in emergency departments (EDs) and neurologic settings. The Fundus Photography vs
Ophthalmoscopy Trial Outcomes in the Emergency Department (FOTO-ED) study showed
that ED providers consistently failed to correctly identify relevant ocular funduscopic findings
using the direct ophthalmoscope, and that nonmydriatic fundus photography was an effective
alternate way of providing access to the ocular fundus in the ED. Extrapolating these results to
headache clinics, outpatient neurology clinics, and adult and pediatric primary care settings
seems self-evident. As technology advances, nonmydriatic ocular fundus imaging systems will
be of higher quality and more portable and affordable, thereby circumventing the need to
master the use of the ophthalmoscope. Visualizing the ocular fundus is more important than the
method used. Ocular fundus photography facilitates nonophthalmologists’ performance of this
essential part of the physical examination, thus helping to reestablish the value of doing so.

*These authors contributed equally to this work.

From the Departments of Ophthalmology (V.B., B.B.B., N.J.N.), Neurology (V.B., B.B.B., N.J.N.), Epidemiology (B.B.B.), and Neurological Surgery (N.J.N.), Emory University School of
Medicine, Atlanta, GA.

Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Copyright © 2017 American Academy of Neurology 1


Copyright ª 2017 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
Glossary
ACEP = American College of Emergency Physicians; ACGME = Accreditation Council for Graduate Medical Education; CI =
confidence interval; ED = emergency department; FOTO-ED = Fundus Photography vs Ophthalmoscopy Trial Outcomes in
the Emergency Department; IIH = idiopathic intracranial hypertension.

Case history 1 diversion, her vision improves only slightly and she remains
legally blind.
A 28-year-old woman presents to an emergency department
(ED) with severe headache, neck pain, and nausea. Her ex-
amination is recorded as normal; she is diagnosed with mi- Case history 2
graine headaches, treated with analgesics, and sent home.
Two weeks later, she returns to the same ED complaining of A 20-year-old woman goes to an ED with severe headache,
continued headaches and new blurred vision in both eyes. neck pain, and nausea. Her chief complaint of headache
Examination is again recorded as normal and a CT scan of triggers the acquisition of ocular fundus photographs on
the head without contrast is unremarkable. She is diagnosed a nonmydriatic fundus camera in the ED as part of a research
again with migraine, and sent home with an outpatient study on the feasibility and usefulness of fundus photographs
neurology referral. A week later, she is seen in an outpatient during routine ED care (figure 2). The photographs are
neurology clinic, where an electronic medical record indi- uploaded into the electronic medical record where they are
cates a normal neurologic examination, including normal viewed by the ED provider and recognized as showing pap-
cranial nerves, and she is referred for outpatient ophthal- illedema. This is confirmed by telemedical assessment of the
mologic evaluation. By the time she sees the ophthalmolo- photographs remotely by an ophthalmologist. The patient’s
gist the following week, her vision is recorded as no workup occurs immediately in the ED and neuro-
perception of light in the right eye and perception of light ophthalmologic evaluation confirms the diagnosis of IIH
only in the left eye, with bilateral severe papilledema on and the need for immediate neurosurgical management. The
ocular funduscopic examination (figure 1). She is sent patient maintains excellent central visual acuity with mild
emergently to the ED, where a brain MRI and magnetic peripheral visual field deficits, none of which remains symp-
resonance venography are normal with the exception of ra- tomatic or functionally limiting.
diographic signs of elevated intracranial pressure1 and
a lumbar puncture confirms an elevated opening pressure of
>55 cm H2O with otherwise normal CSF contents, estab-
Scope of the problem
lishing the diagnosis of idiopathic intracranial hypertension In 1851, by the light of a candle, Hermann von Helmholtz
(IIH).2,3 Despite immediate surgical intervention for CSF viewed the living human ocular fundus via direct

Figure 1 Ocular fundus shows severe bilateral papilledema

2 Neurology | Volume 90, Number 4 | January 23, 2018 Neurology.org/N


Copyright ª 2017 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
pressure altered patient disposition and contributed to the
Figure 2 Fundus photographs as seen on the patient’s final diagnosis, confirming the importance of funduscopic
electronic medical records, showing severe bi- examination in the ED.8
lateral papilledema
It is not surprising that ophthalmoscopy was eventually in-
corporated into medical education.6,7,9 Examination of the ocular
fundus has always been an integral part of the neurologic
examination.4,6 The standard core curriculum for medical stu-
dents’ neurologic clerkship10,11 cites funduscopic examination as
one of the elements of the neurologic examination that must be
taught during the neurology clerkship. Funduscopic examination
is also listed in the Neurology Residency Core Curriculum.12,13
In addition, the Accreditation Council for Graduate Medical
Education (ACGME) Neurology and Pediatric Neurology
Milestones includes “visualizes papilledema” as a Neurologic
Examination Milestone.14 Although neither the American
Academy of Neurology Headache & Facial Pain Fellowship
Core Curriculum15 nor the United Council for Neurologic
Subspecialties Headache Medicine Core Curriculum16 specifi-
cally mentions this skill, it is implicitly included in the neurologic
examination and is of crucial importance in excluding papil-
ledema during the evaluation of a patient with headache. Simi-
larly, the Model of the Clinical Practice of Emergency Medicine
(an outline for the core knowledge base required of emergency
physicians revised in 201617 and adopted by all 6 national
organizations of emergency medicine) lists headache and pap-
ophthalmoscopy and ushered in a new era in the field of illedema as 2 of the critical symptoms or signs (defined as “a
ophthalmologic diagnosis.4–6 In addition to the obvious symptom or sign of a life-threatening illness or injury with a high
importance of viewing the ocular fundus in patients with probability of mortality if immediate intervention is not begun to
visual complaints, it became clear by the late 19th century prevent further…neurologic instability”) the knowledge of
that findings seen on ocular fundus examination could crit- which must be mastered by emergency medicine specialists.
ically inform the diagnosis of neurologic and systemic dis- Although this article does not specifically mention examination
eases and alter acute and chronic management.5 Despite the of the ocular fundus in the list of skills integral to the practice of
subsequent invention of other methods of examining the emergency medicine, which does include slit-lamp examination,
back of the eye, such as indirect ophthalmoscopy and the same document lists headache, idiopathic intracranial hy-
slit-lamp biomicroscopy with lens magnification,2 direct pertension, and cerebral venous thrombosis among the critical
ophthalmoscopy remained essentially the only clinical ex- disorders commonly encountered in emergency medicine, in-
amination technique to view the ocular fundus available to dicating that identification of papilledema in the ED is an es-
nonophthalmologic physicians. Ophthalmoscopy became sential part of the clinical examination.17 The ACGME
integrated into the general physical examination performed milestones18 emphasize the ability to perform a physical exam-
by physicians, especially those specializing in primary care, ination, recognize pertinent physical findings, and perform
pediatrics, internal medicine, neurology, neurosurgery, and techniques required for conducting the examination. A wall-
emergency medicine.6,7 mounted or portable ophthalmoscope is listed among the sug-
gested equipment for EDs proposed by the American College of
Examination of the ocular fundus provides a unique oppor- Emergency Physicians (ACEP).19 The ACEP-endorsed clinical
tunity to directly view CNS tissue and its vasculature. De- policy statement on the evaluation and management of adult
tection of retinal vascular occlusions, hypertensive and patients presenting to the ED with acute, nontraumatic head-
diabetic retinopathy, and red flags for neurologic disorders ache, last updated in 2008,20 emphasizes that “the cornerstone of
such as optic disc swelling or pallor not only facilitates ap- assessing the patient with headache is the medical history and
propriate management of a vision-threatening condition, but physical examination.” This policy states that “adult patients with
often reveals an underlying systemic or neurologic disease headache and exhibiting signs of increased intracranial pressure
that has dire implications for a patient’s well-being and that (e.g., papilledema, absent venous pulsations on funduscopic
otherwise would have been overlooked.2,3 examination …) should undergo a neuroimaging study before
having a lumbar puncture in the ED.”20
For example, detection of optic disc edema in 2.6% of 1,408
patients presenting to an ED with a chief complaint of Vision changes necessitate a thorough examination of the eye.
headache, neurologic deficit, visual loss, or elevated blood Most medical specialty societies agree that headaches, acute

Neurology.org/N Neurology | Volume 90, Number 4 | January 23, 2018 3


Copyright ª 2017 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
neurologic deficits, and severely elevated systemic blood of difficult examination skills.31 Although the convenience of
pressure measurements also deserve an assessment of the the instruments and the optical quality of the equipment have
ocular fundus. Yet it is remarkable how infrequently the ocular improved over the years, direct ophthalmoscopy is still a skill
fundus is examined in situations that are nearly universally that necessitates extensive training, practice, and mainte-
acknowledged as requiring this important element of the nance. It requires having the instrument at hand in good
physical examination.6,21–23 Headache is the fourth most working order, with well-charged batteries, a cooperative pa-
common chief complaint among all patients presenting to the tient who can maintain fixation, and a physical setting that
ED and the single most common neurologic complaint,24 but allows for close proximity to both sides of the patient, often
very few studies have evaluated the frequency of ophthal- a problem in an ED or hospital locale. The patient’s pupil
moscopy and abnormal ocular findings in headache patients. must be of adequate size for viewing or pharmacologic di-
A 2008 study25 reported that funduscopic examination was lation is needed, and the room lights are best dimmed, which
performed in 48% of 91 adult patients presenting to an ED is not always possible.2 Pharmacologic dilation of the pupil,
with sudden, severe headache, but whether the ED providers’ routinely utilized by ophthalmologists in their examination of
interpretations of the funduscopic findings were accurate is the ocular fundus, is almost never performed in non-
unknown. The authors proposed an algorithm for emergency ophthalmic settings, largely due to lack of access to dilating
evaluation of severe headache, which included systematic drops, fear of side effects, and reluctance to wait the necessary
examination of the ocular fundus. A 2013 study26 reported 30 minutes for adequate pupillary dilation. Ophthalmoscopy
that only 28 of 228 (12%) patients presenting to the ED with takes longer than most elements of the physical examination,
a chief complaint of headache had direct ophthalmoscopy and it is rare these days for a physician to not feel time
performed by ED providers and that none of the ocular pressure during patient encounters.32 Preceptors of medical
fundus abnormalities such as papilledema, optic nerve pallor, students, residents, fellows, and junior faculty, especially those
or grade IV hypertensive retinopathy present in 8.5% of these who were not themselves well-trained or who are not skilled
headache patients were detected by the ED providers. Con- in the procedure, may actually discourage the practice of di-
sidering that over 3 million patients visit an ED for headache rect ophthalmoscopy among their trainees.21,33,34 In addition,
each year in the United States,27,28 undetected diagnostically even if the ocular fundus is visualized, many non-
relevant ocular fundus findings may be present in more than ophthalmology practitioners do not recognize what they see
250,000 of them. Considering that a large number of patients or appreciate the implications of what they observe.6
with headache and optic nerve head edema have normal brain
imaging or may not be imaged, examination of the ocular
fundus in all headache patients is essential.2,3
How can technology help us?
Reports on the frequency of ocular funduscopic examination Although there are reasonable concerns about advancements
vary according to the examiner’s medical specialty and train- in medical technology contributing to a decline in clinician
ing level and the patient encounter type. Even neurologists examination skills,35 innovations in medical technology are
often fail to examine the ocular fundus. A pilot study of 163 one of the driving forces for innovation in medicine. Ocular
headache patients evaluated in the ED, in inpatient units, or in fundus photography takes advantage of improvements in
outpatient clinics revealed that funduscopy was performed in imaging technology to circumvent the technical obstacle of
only 11% of patients examined by an internal medicine spe- viewing the ocular fundus with an ophthalmoscope. Retinal
cialist, 20% of patients examined in the ED, and 43% of photography was first introduced in 1886 (shortly after the
patients examined by a neurologist.29 However, despite fun- ophthalmoscope was first used), became commercially avail-
duscopy being an essential part of any full neurologic exam- able in 1926, and has been routinely used since the 1950s.36,37
ination, funduscopy is rarely if ever performed.6,7,21–23 In The continued development of the technology has culmi-
a 2010 study of 92 patients presenting to an urgent care center nated in nonmydriatic high-resolution digital fundus pho-
with acute medical conditions for which funduscopy would be tography. Compact and user-friendly tabletop and handheld
clinically relevant, only 15% of patients had an examination of digital cameras provide very high-quality photographs show-
the ocular fundus performed.22 In a study evaluating the ing the entire ocular fundus even without pharmacologic di-
overdiagnosis of IIH, 20% of care providers consulted for lation of the pupils (figure 3).36–38 The most recent cameras
headaches did not attempt to perform ophthalmoscopy, while can directly connect to electronic medical records, allowing
44% of those who examined the ocular fundus misinterpreted immediate and secure transmission of images.37,39,40 Portable
the optic nerve appearance as papilledema.30 smartphone-based ophthalmic cameras combined with
applications have also emerged.37

Barriers to adequate performance of Although most smartphone photography to date does not
provide high-quality nonmydriatic retinal imaging, expected
the ocular funduscopic examination technical improvements will soon likely allow these cameras
Performing direct ophthalmoscopy is not easy. Ocular fundus to replace the outdated direct ophthalmoscope in the pocket
examination is listed second in the Stanford Medicine 25 list of any medical care provider.

4 Neurology | Volume 90, Number 4 | January 23, 2018 Neurology.org/N


Copyright ª 2017 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
accepted as warranting ocular fundus examination. All in-
Figure 3 Normal nonmydriatic ocular fundus photograph cluded patients had nonmydriatic ocular fundus photographs
of the left eye with an inset showing the typical taken by nurse practitioners or a medical student after an
field of view of a direct ophthalmoscope
average of 10 minutes of training using a commercially
available nonmydriatic tabletop digital ocular fundus camera.
Photographs were taken at the time of triage in a lighted room
and were transmitted electronically to a neuro-
ophthalmologist for remote interpretation. Relevant ocular
fundus abnormalities were defined as optic disc edema, iso-
lated intraocular hemorrhage, grade III or IV hypertensive
retinopathy, retinal vascular occlusion, and optic disc pallor,
findings that would change patient ED management and
disposition (figure 4 and table).

The first phase of the FOTO-ED study evaluated the routine


clinical use of direct ophthalmoscopy by ED providers.43 The
photographs were not made accessible to the ED providers
whose behavior regarding examination of the ocular fundus
with an ophthalmoscope and interpretation of findings was
recorded by an external observer. This phase demonstrated
that direct ophthalmoscopy was infrequently and poorly
performed by ED providers. Review of the fundus photo-
graphs by a neuro-ophthalmologist revealed relevant ocular
findings in 44 of the 350 enrolled patients (13%; 95% confi-
dence interval [CI] 9%–17%). The ED providers only per-
formed ocular funduscopic examination using a direct
One of the obvious advantages of digital imaging is the
ophthalmoscope in 48 of the 350 enrolled patients (14%; 95%
possibility of immediate transfer of imaging for remote
CI 10%–18%). Eleven of the 44 relevant findings were known
interpretation. Numerous studies have validated the use of
prior to the ED evaluation and an additional 6 were identified
tele-ophthalmology in primary care centers, with remote in-
by an ophthalmologist during a consultation in the ED,
terpretation of retinal photographs to screen for numerous
leaving 27 patients with relevant findings on photography
ocular diseases such as diabetic retinopathy.41 The same can
who neither had an ophthalmology consultation requested
be done for fundus abnormalities relevant to ED care or
nor were diagnosed by the ED providers. Thus, 82% (95% CI
neurology clinical practice, with appropriate interpretation of
65%–93%) of the findings unknown at the time of pre-
transmitted images easily accomplished on the go using
sentation to the ED were missed by routine ED care, and the
a smartphone or a tablet.40 The image quality of nonmydriatic
ED providers themselves missed 100% of the relevant find-
fundus photographs on an iPhone 3G was found to be su-
ings, even when they tried to use the direct ophthalmoscope,
perior to that of the same photographs on a desktop com-
which was infrequently. This first phase of the FOTO-ED
puter,42 likely because of the advanced features of the
study clearly demonstrated the superiority of nonmydriatic
smartphone’s display and the ease of enlarging and moving
fundus photography interpreted by neuro-ophthalmologists
images on a smartphone. Smartphones can also video dy-
to routine direct ophthalmoscopy by ED providers. The study
namic phenomena such as spontaneous venous pulsations,
also showed that nonmydriatic fundus photography was fea-
and new image processing software can accurately reproduce
sible in the ED without altering ED routine flow.44 Both
various retinal findings and screen for abnormalities based on
patients and those taking the photographs found the process
artificial intelligence–driven algorithms.37
agreeable and brief (mean ease, speed, and comfort rating
≥8.7 out of 10 for all; median photography time, 1.9 minutes;
interquartile range 1.3–2.9 minutes, representing less than
The FOTO-ED 3-phase study 0.5% of the patient’s total ED visit time). The photographs
The Fundus Photography vs Ophthalmoscopy Trial Out- were of good quality and provided adequate examination of
comes in the Emergency Department (FOTO-ED) study the ocular fundus to allow for identification of relevant find-
evaluated whether nonmydriatic ocular fundus photography ings in 97% of enrolled patients in at least one eye.45
would be feasible and would improve diagnosis and patient
disposition in the ED compared with direct The second phase of the FOTO-ED study evaluated the
ophthalmoscopy.43–47 The FOTO-ED study included patients routine use of nonmydriatic ocular fundus photography as
presenting to a university hospital ED with headaches, focal interpreted by the ED providers.46 The photographs were
neurologic deficits, acute visual changes, or diastolic blood automatically transferred into the ED folder of the patient’s
pressure ≥120 mm Hg, symptoms and signs generally electronic medical record and the ED providers were alerted

Neurology.org/N Neurology | Volume 90, Number 4 | January 23, 2018 5


Copyright ª 2017 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
Figure 4 Pie chart shows the distribution of the 153 (11.8%) relevant findings observed among 1,291 patients enrolled in
the 3 phases of the Fundus Photography vs Ophthalmoscopy Trial Outcomes in the Emergency Department
(FOTO-ED) study

The photographs in each slice were taken during the study.

that photographs were available by an eye icon appearing on findings on ocular fundus photographs. Trained ED providers
the list of tests performed for each patient. There was no reviewed 45% of photographs and correctly identified ab-
incentive to encourage the ED providers to open the pho- normal images in 67% of cases and normal images in 80% of
tography folder and the ED providers did not receive any cases before training, compared with 43%, 45%, and 83%,
specific education regarding how to interpret fundus photo- respectively, after training. Untrained ED providers reviewed
graphs. Of the 354 enrolled patients in phase II, 35 (10%; 95% 35% of photographs and correctly identified abnormal find-
CI 7%–13%) had relevant findings identified on the fundus ings in 50% of cases and normal images in 79% of normal
photographs by a neuro-ophthalmologist. The ED providers cases. This study confirmed that ED providers perform much
reviewed the photographs in 239 patients (68%), which was better with fundus photography than with direct ophthal-
much higher than their 14% frequency of examination of the moscopy, especially to identify normal fundus photographs.
ocular fundus with the direct ophthalmoscopy in phase I. However, the in-service training did not result in significant
Importantly, they identified relevant abnormalities in 16 of 35 improvement in the interpretation of these photographs.
patients (sensitivity 46%; 95% CI 29%–63%), which was also
much better than the 0% detection rate with only the direct The 3 phases of the FOTO-ED study clearly showed that
ophthalmoscope in phase I. The ED providers also correctly most ED providers consistently fail to correctly identify rel-
identified 289 of 319 ocular fundus photographs as normal evant ocular funduscopic findings using the direct ophthal-
(specificity 96%; 95% CI 87%–94%), which they believed was moscope, and that nonmydriatic fundus photography is an
particularly helpful (e.g., allowing exclusion of papilledema in effective alternate way of providing access to the ocular fundus
a patient with headaches). in the ED. A total of 1,291 patients were included in the 3
phases of the FOTO-ED study, among whom 153 (12%) had
The third phase of the FOTO-ED study was a quality im- relevant findings on fundus photographs that altered the ED
provement project performed to determine whether a 30- management of these patients. The ED providers were not
minute web-based educational module would improve the ED able to identify any of the relevant findings in phase I without
providers’ performance.47 Consistent with previous phases of the help of an ophthalmologist consultant, but they recog-
the FOTO-ED study, 12.6% (74) of the 587 patients pre- nized 40 of the 109 (36.7%) relevant findings when given
senting to the ED with eligible chief complaints had relevant access to fundus photographs in phases II and III. They also

6 Neurology | Volume 90, Number 4 | January 23, 2018 Neurology.org/N


Copyright ª 2017 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
Table Emergency department (ED) providers’ performance with ocular funduscopic examination in the 3 phases of the
Fundus Photography vs Ophthalmoscopy Trial Outcomes in the Emergency Department (FOTO-ED) studies
Phase I (direct Phase II (nonmydriatic Phase III (web-based in-
ophthalmoscopy) photography) service training)

Patients, n 350 354 587

Age, y, median (interquartile range) 45 (31–59) 46 (33–57) 46 (34–61)

Women, n (%) 220 (63) 251 (71) 392 (67)

Chief complaints, n (%)a

Headache 228 (65) 206 (58) 308 (52)

Focal neurologic deficit 100 (29) 123 (35) 181 (31)

Visual changes 92 (26) 56 (16) 65 (11)

DBP ≥120 mm Hg 21 (6) 21 (6) 101 (17)

Relevant findings, n (%) 44 (13) 35 (10) 74 (13)

Optic disc edema 13 6 20

Grade III/IV hypertensive retinopathy 10 6 9

Isolated intraocular hemorrhage 13 7 16

Optic disc pallor 4 15 24

Retinal vascular occlusion 4 1 5

ED physician fundus examination technique Direct ophthalmoscopy Nonmydriatic photography Nonmydriatic photography

Patients whose ocular fundus was viewed by ED 48 (14) 239 (68) 237 (40)
physicians, n (%)

Abnormalities correctly detected by ED physician 0 (0) 16 (46) 24 (32)


examination, n (%)

Abbreviation: DBP = diastolic blood pressure.


a
These sum to more than 100% because patients were allowed to report more than one complaint.

correctly identified 448 out of the 515 (87%) normal images, The applications of this technology in neurology settings are
which was believed to be very helpful, particularly in patients multiple and go beyond the assessment of papilledema in
with headaches in whom papilledema could be easily and headache patients. For example, recognition of grade III/IV
reliably excluded. hypertensive retinopathy is important in numerous neuro-
logic emergencies.43,53,54 Ocular fundus photography may also
Future applications prove useful in the risk stratification of patients presenting
with suspected TIA or stroke48,55–57 or in critically ill patients
The FOTO-ED study triggered a great deal of interest and in whom identification of ocular fundus abnormalities may
enthusiasm not only from ED providers, but medical students, affect acute management and prognosis.58
residents, and nonophthalmology physicians such as neurol-
ogists. Indeed, the findings of the FOTO-ED study can likely New inexpensive, portable, easy-to-operate fundus cameras
be extrapolated to other nonophthalmologic settings.48,49 have revolutionized retinal screening programs, which have
Numerous other studies have now validated the use of cam- grown exponentially over the last decade. Tele-
eras in clinical settings other than adult EDs.50–54 The feasi- ophthalmology screening is now the standard of care in
bility and reliability of nonmydriatic fundus photography in linking remote areas to ophthalmologists.41 Neurology clinics,
children as young as 22 months was demonstrated in a pedi- primary care offices, urgent care centers, and EDs can use any
atric ophthalmology clinic.50 A subsequent study validated the of the nonmydriatic cameras that connect directly to elec-
use of a tabletop nonmydriatic camera in children ages 5–12 tronic medical records and integrate fundus photographs into
years in a pediatric ED.51 Another study showed that relatively a patient’s systematic evaluation. Although the hope is that
good images of the optic disc could be obtained in children as most physicians will learn to accurately interpret the photo-
young as 2 years without pupillary dilation using a smart- graphs themselves, remote interpretation by an ophthalmol-
phone attached to an ophthalmoscope.52 ogist is always possible, facilitated by the integrated Internet

Neurology.org/N Neurology | Volume 90, Number 4 | January 23, 2018 7


Copyright ª 2017 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
connection capability of most recent cameras. Obtaining EY006360), NIH (R01-NS089694), and Research to
a fundus photograph does not replace an ophthalmologic Prevent Blindness. B. Bruce served as a consultant for Med-
consultation in patients with visual complaints, when the di- Immune (data safety and monitoring board) and Bayer
agnosis is not obvious, or when the photograph is of poor (medicolegal), has provided expert testimony on optic disc
quality. Rather, such photographs should be considered an edema, and received research support via his institution from
integral part of the clinical examination that should prove Teva Pharmaceuticals, Pfizer, Novartis, and the NIH (P30-
helpful in triaging patients appropriately. EY006360, R01-NS089694). N. Newman is a consultant for
Gensight Biologics (France) and Santhera Pharmaceuticals
The new generation of medical students embraces new (Switzerland), serves on the Data Safety Monitoring Board
technology and already prefers nonmydriatic fundus pho- for a Quark Pharmaceuticals (Israel) clinical trial, has pro-
tography to direct ophthalmoscopy.33,34,49 Obtaining a pho- vided expert testimony on optic disc edema, and has received
tograph in a few seconds instead of trying to visualize the research support from NIH grants (R01-089694, P30-
ocular fundus with a direct ophthalmoscope allows providers EY006360) and Research to Prevent Blindness Lew R. Was-
to focus on the findings and their implications for diagnosis serman Merit Award. Go to Neurology.org/N for full
and management rather than on the technique of mastering disclosures.
ophthalmoscopy. Traditional medical school and residency
curricula should include interpretation of ocular fundus Received July 24, 2017. Accepted in final form October 5, 2017.
photography as an educational tool.49 Restoring the ocular
fundus examination to its appropriate place in general and References
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possible for nonophthalmologists to easily visualize the ocular 11. American Academy of Neurology, Association of University Professors of Neu-
fundus in a timely fashion and reestablishes the value of do- rology, American Neurological Association. Neurology clerkship core curriculum
guidelines. Available at: aan.com/uploadedFiles/4CME_and_Training/2Training/
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at: acgme.org/Specialties/Milestones/pfcatid/37/Neurology. Accessed September
Author contributions 25, 2017.
Valérie Biousse: participated in the design of the study, in the 13. American Board of Psychiatry & Neurology. Neurology core competencies outline.
2000. Available at: abpn.com/wp-content/uploads/2015/02/2011_core_N_MREE.
analysis and interpretation of the data, and in the drafting and pdf. Accessed September 25, 2017.
critical revision of the manuscript. Beau B. Bruce: participated 14. The Accreditation Council for Graduate Medical Education, The American Board of
Psychiatry and Neurology. The neurology milestone project. 2015. Available at:
in the design of the study, in the collection, analysis, and acgme.org/Specialties/Milestones/pfcatid/37/Neurology. Accessed September 25,
interpretation of the data, and in the critical revision of the 2017.
manuscript. Nancy J. Newman: participated in the design of 15. Headache and Facial Pain Fellowship Core Curriculum (American Academy of
Neurology). Available at: aan.com/uploadedFiles/Website_Library_Assets/Docu-
the study, in the analysis and interpretation of the data, and in ments/8Membership/3People/5Sections/1Drop_down_for_33_sections/Head-
the drafting and critical revision of the manuscript. ache_and_Facial_Pain/Fellowship%20Core%20Curricula.pdf. Accessed September
25, 2017.
16. United Council for Neurologic Subspecialties. Headache medicine core curricu-
Study funding lum. Available at: ucns.org/globals/axon/assets/3672.pdf. Accessed September 25,
2017.
Supported in part by Research to Prevent Blindness (De- 17. Counselman FL, Babu K, Edens MA, et al; 2016 EM Model Review Task Force,
partment of Ophthalmology) and NIH grants P30-EY006360 Beeson MS, Keehbauch JN; American Board of Emergency Medicine. The 2016
model of the clinical practice of emergency medicine. J Emerg Med 2017;52:846–849.
(Department of Ophthalmology), K23-EY019341 (B. Bruce), 18. The Accreditation Council for Graduate Medical Education, The American Board of
and UL1-RR025008 (V. Biousse). Emergency Medicine. The emergency medicine milestone project. 2015. Available at:
acgme.org/Specialties/Milestones/pfcatid/7/Emergency%20Medicine. Accessed
September 25, 2017.
Disclosure 19. American College of Emergency Medicine. Emergency department planning and
resource guidelines. 2014. Available at: acep.org/uploadedFiles/ACEP/Practice_R-
V. Biousse is a consultant for Gensight Biologics (France) and esources/policy_statements/ED_Planning_Policy_FINAL_040914.pdf. Accessed
received research support from the NIH/PHS (P30- September 25, 2017.

8 Neurology | Volume 90, Number 4 | January 23, 2018 Neurology.org/N


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