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GRANT L. HOWELL, GERMÁN CHÁVEZ, COLIN A. MCCANNEL, PETER A. QUIROS, SABA AL-HASHIMI, FEI YU,
SIMON FUNG, CHRISTOPHER M. DEGIORGIO, YUE MING HUANG, BRADLEY R. STRAATSMA,
CLARENCE H. BRADDOCK, AND GARY N. HOLLAND
• OBJECTIVE: To compare results of simulator-based vs ulator group (median: 5.0, range: 0.0-11.0) than for the
traditional training of medical students in direct ophthal- traditional group (median: 4.0, range: 0.0-9.0), although
moscopy. the difference was not significant. The simulator group
• DESIGN: Randomized controlled trial. was less likely to mistake the location of a macular scar
• METHODS: First-year medical student volunteers com- in 1 patient (odds ratio: 0.28, 95% confidence interval:
pleted 1 hour of didactic instruction regarding direct oph- 0.056-1.35, P = .013).
thalmoscopes, fundus anatomy, and signs of disease. Stu- • CONCLUSIONS: Direct ophthalmoscopy is difficult, re-
dents were randomized to an additional hour of training gardless of training technique, but simulator-based train-
on a direct ophthalmoscope simulator (n = 17) or super- ing has apparent advantages, including improved tech-
vised practice examining classmates (traditional method, nique, the ability to localize fundus lesions, and a foster-
n = 16). After 1 week of independent student prac- ing of interest in learning ophthalmoscopy, reflected by
tice using assigned training methods, masked ophthalmol- increased practice time. (Am J Ophthalmol 2022;238:
ogist observers assessed student ophthalmoscopy skills 187–196. © 2021 The Authors. Published by Elsevier
(technique, efficiency, and global performance) during Inc.
examination of 5 patient volunteers, using 5-point Lik- This is an open access article under the CC BY-NC-ND
ert scales. Students recorded findings and lesion location license
for each patient. Two masked ophthalmologists graded (http://creativecommons.org/licenses/by-nc-nd/4.0/))
answer sheets independently using 3-point scales. Stu-
dents completed surveys before randomization and after
D
assessments. Training groups were compared for grades, irect ophthalmoscopy allows clinicians, regardless
observer- and patient-assigned scores, and survey re- of specialty, to visualize fundus findings, includ-
sponses. ing diabetic retinopathy and papilledema, that are
• RESULTS: The simulator group reported longer practice critical for the evaluation of patients with systemic disor-
times than the traditional group (P = .002). Observers ders. The Association of University Professors of Ophthal-
assigned higher technique scores to the simulator group mology recommends that all medical students learn to ap-
after adjustment for practice time (P = .034). Combined preciate anatomic landmarks and signs of disease through
grades (maximum points = 20) were higher for the sim- direct ophthalmoscopy.1 Nevertheless, studies report that
medical students, nonophthalmology residents, and prac-
ticing physicians lack confidence in their ophthalmoscopy
Supplemental Material available at AJO.com.
skills.2-4 Both educators and trainees attribute the lack
Accepted for publication November 9, 2021. of skill, in part, to inadequate training during medical
UCLA Stein Eye Institute, David Geffen School of Medicine at UCLA, school.5 , 6 In a survey of residency program directors in pri-
University of California, Los Angeles; Department of Ophthalmology, mary care specialties, respondents felt that medical schools
David Geffen School of Medicine at UCLA, University of California, Los
Angeles; UCLA Simulation Center, David Geffen School of Medicine were not training students adequately to perform direct
at UCLA, University of California, Los Angeles; Doheny Eye Institute, ophthalmoscopy once they are in residencies.6
Pasadena; Departments of Neurology, Cardiology, and Neurobiology, Traditionally, teaching direct ophthalmoscopy skills in-
David Geffen School of Medicine at UCLA, University of California, Los
Angeles, California, USA; Department of Anesthesiology and Periopera- volves student-on-student (or student-on-patient) practice;
tive Medicine, David Geffen School of Medicine at UCLA, University of however, such instruction involves many challenges that
California, Los Angeles, California, USA; Office of the Dean, David Gef- limit its educational value, including an inability to pro-
fen School of Medicine at UCLA, University of California, Los Angeles,
California, USA; Department of Biostatistics, UCLA Jonathan and Karin vide students with accurate feedback about what they have
Fielding School of Public Health, Los Angeles seen in the fundi of examinees.7 Studies have evaluated al-
Inquiries to Gary N. Holland, UCLA Stein Eye Institute, 100 ternative teaching techniques, including use of “teaching”
Stein Plaza, UCLA, Los Angeles, CA 90095-7000, USA.; e-mail:
uveitis@jsei.ucla.edu ophthalmoscopes, which provide instructors with images of
© 2021 THE AUTHORS. PUBLISHED BY ELSEVIER INC.
0002-9394/$36.00 THIS IS AN OPEN ACCESS ARTICLE UNDER THE CC BY-NC-ND LICENSE 187
https://doi.org/10.1016/j.ajo.2021.11.016 (HTTP://CREATIVECOMMONS.ORG/LICENSES/BY-NC-ND/4.0/).
what students see; fundus photography; and direct ophthal- technique, and common mistakes made by students learn-
moscope simulators.8-12 Simulation has been shown to im- ing to use the ophthalmoscope). Signs of retinal disease in-
prove surgical skills among residents,13-15 but evidence is cluded examples similar to those in study eyes of patient
limited regarding the value of simulation for teaching direct volunteers, but were not limited to those signs; examples
ophthalmoscopy to students.12 In this article, we describe included papilledema, large optic disc cups, chorioretinal
the results of a randomized controlled trial that compared scars, drusen, signs of vasculopathies and ischemia (hem-
simulator-based vs traditional teaching of direct ophthal- orrhage, cotton-wool spots, exudates), and nevi. Students
moscopy to first-year medical students. in each session had been randomized 1:1 into simulator
and traditional training groups using block randomization,
but assignments for each day were revealed after didactic
instruction. All participants on a given day attended the
same didactic session, regardless of randomization assign-
METHODS ment. Didactic sessions were conducted by the same in-
structor each day (G.N.H.). Training groups ranged in size
This prospective, randomized, controlled trial was con-
from 4 to 8 students.
ducted at the David Geffen School of Medicine at UCLA.
The simulator group was introduced to the Eyesi Direct
First-year medical student volunteers were recruited in May
Ophthalmoscope Simulator (Model EDO491 #03 × 0127,
2019 to participate in the study via e-mail and social media
Platform 2.1, Software v1.8.0.113443; VRmagic GmbH,
announcements. Students were not eligible for participa-
Mannheim, Germany) during an additional hour by 1 fac-
tion in the trial if they had had more than an introduc-
ulty instructor (C.A.M.) and a manufacturer’s representa-
tory demonstration of the direct ophthalmoscope or had
tive. The simulator contains 4 “modules,” each with numer-
practiced use of a direct ophthalmoscope independently.
ous “cases” that are scored on the operator’s ability to com-
Meals were provided at study sessions, and students were
plete tasks.16 The first 2 modules focus on finding geomet-
given $50 Amazon gift cards on study completion. Five pa-
ric shapes superimposed on a simulated fundus. The simu-
tient volunteers with various fundus findings were recruited
lator registers whether the operator successfully locates the
from faculty practices to participate in the assessment phase
shape. A cross hair indicating the position of gaze must be
of the study. Patients were given $100 Amazon gift cards
held over the shape for 1 second for the simulator to regis-
for participation. Seven ophthalmologists with experience
ter it as having been “seen.” The simulator also records and
in medical student instruction volunteered to assess stu-
displays a map of the total fundus area that has been viewed,
dent performance; 5 evaluated students as they examined
thereby promoting efficient scanning of the entire posterior
patients (see Acknowledgments) and 2 (P.A.Q., S.A.-H.)
pole. Each student in the simulator group used the first mod-
graded answer sheets on which students recorded their
ule during the training hour. The third and fourth modules
findings. Fundus imaging of the study eye of each patient
display simulated pathologic retinal and optic disc lesions.
had been performed with photography or optical coher-
The fourth (examination) module evaluates the operator’s
ence tomography to assist in grading student answer sheets
ability to identify lesions and was not available to students
(Figure 1). All assessments were masked to each student’s
during the study. The simulator also addresses some aspects
training group. The study was approved by the UCLA Insti-
of the direct ophthalmoscopy technique. Some cases re-
tutional Review Board before participant recruitment and
quire operators to adjust “lenses” within the ophthalmo-
data collection.
scope hand piece to obtain a clear view of the simulated fun-
dus; another penalizes operators unless the fundus is viewed
• DATA COLLECTION AND STUDY PROCEDURES: The through simulation of an undilated pupil.
study was conducted in 3 phases: training, practice, and During the same hour, the traditional training group ex-
skills assessment. Students completed a pretraining survey amined fellow students with their personal direct ophthal-
that collected the following information: prior direct oph- moscopes under the guidance of 2 faculty instructors (S.F.,
thalmoscopy experience (yes vs no), prior study of eye dis- G.N.H.). Pupillary dilation of examined students was op-
ease (yes vs no), and the presence or absence of pre-existing tional. After training, all students were encouraged to prac-
eye conditions (refractive error corrected by glasses or con- tice ophthalmoscopy independently, using only their as-
tact lenses, color-blindness, amblyopia). Investigators not signed training method (practice on the simulator vs prac-
involved in training or assessments randomized (F.Y.) and tice on family members, friends, or fellow students).
enrolled (G.C.) student volunteers. All students were assessed at a single session, 4 days af-
Training was conducted in 3 identical sessions on con- ter the final training day. Students were placed in ran-
secutive days. The session in which each student could par- dom order to begin assessments. Patient volunteers were
ticipate was dictated by other school responsibilities. Train- placed in 5 examination lanes. Study eyes were dilated with
ing began with a 1-hour didactic session on fundus anatomy, tropicamide 1% and phenylephrine 2.5%. Before examina-
signs of retinal and optic disc disease, and basic principles of tions, students were oriented to an answer sheet on which
direct ophthalmoscopy (ophthalmoscope controls, proper they were to record (1) abnormal findings in the posterior
pole and (2) location of those findings on fundus diagrams ined, but no further instructions were given. Students were
printed on the answer sheet. Students were asked to de- told not to reveal their training technique to observers or
scribe lesion characteristics (size, color, and shape) in their patients, and patients had been told not to reveal their eye
own words. Diagnoses were not required. Two additional problems to students. Both observers and patients were told
options were “normal fundus,” if they found no abnormali- not to provide students with feedback during the examina-
ties, and “could not visualize fundus.” tion. Students had 1 minute to perform each examination,
Students examined all 5 patient volunteers in the same during which observers assigned them 3 scores (technique,
order; after the first student examined the first patient and efficiency, and global, as described below). After each ex-
moved to the second patient, the second student in line ex- amination, students exited the examination lane and had
amined the first patient, and so forth until each patient had 1 minute to complete answer sheets before moving to the
been examined by every student. A single masked ophthal- next patient. During the same minute, patients assigned a
mologist observer was assigned to each examination lane single global score for student performance, as described be-
for the entire assessment period. On entry into the exami- low. Students were asked not to discuss their answers with
nation lane, students were told which eye was to be exam- other students until all examinations were completed and
Score or Grade Factors Related to Student Performance That Were Appropriate for Assigning Specific Scores and Grades
TABLE 3. Summary Grades Assigned by Masked Ophthalmologist Graders to 33 First-Year Medical Student Participants in a
Randomized Controlled Trial of Training Techniques for Learning Direct Ophthalmoscopy, Based on Examination of 5 Patient
Volunteers.
Grade Simulator Group (n = 17) Traditional Group (n = 16) P Valuea Adjusted P Valueb
Table 5 shows ophthalmologist-observer and patient- not statistically significant (P = .178). Scores did not im-
volunteer scores assigned to students. Observers scores prove in either group as students progressed from patient to
assigned to simulator-trained students were consistently patient (data not included).
higher than scores assigned to traditionally trained students Table 6 summarizes student responses in the postassess-
for technique (P = .011), efficiency (P = .007), and global ment survey. The simulator group reported longer indepen-
performance (P = .004). Technique (P = .034) and global dent practice time than the traditional group (P = .002).
performance (P = .025) scores remained statistically signif- With respect to students’ perceptions of their assigned
icant after adjustment for practice time. Patients assigned training method vs their understanding of the alternative
higher scores to students in the simulator group than to technique, the number of students within each group who
those in the traditional group, although the difference was felt that their method was strictly advantageous was simi-
Gradea Simulator Group (n = 17) Traditional Group (n = 16) P Valueb Adjusted P Valuec
TABLE 5. Summary Scores Assigned by Masked Ophthalmologist Observers to 33 First-Year Medical Student Participants, Based
on Examination of 5 Patient Volunteers, and a Summary Score Assigned to the Students by Those Patient Volunteers in a
Randomized Controlled Trial Comparing Simulator-based vs Traditional Training of Direct Ophthalmoscopy.
Scoresa Simulator Group (n = 16)b Traditional Group (n = 16) P Valuec Adjusted P Valued
Ophthalmologist-observer scores
Technique .011 .034
Mean ± SD 19.1 ± 2.0 16.4 ± 2.8
Median (range) 19.0 (16.0-23.0) 17.0 (11.0-21.0)
IQR 17.5, 21.0 14.0, 18.0
Efficiency .007 .066
Mean ± SD 19.8 ± 2.1 17.1 ± 3.0
Median (range) 20.0 (16.0-22.0) 17.5 (12.5-23.0)
IQR 18.5, 22.0 15.0, 18.5
Global performance .004 .025
Mean ± SD 19.8 ± 1.8 17.2 ± 2.4
Median (range) 20.0 (17.0-23.0) 18.0 (12.5-22.0)
IQR 18.3, 21.0 15.8, 18.8
Patient-volunteer score
Global performance .178 .207
Mean ± SD 21.7 ± 1.3 20.9 ± 1.8
Median (range) 22.0 (19.0-24.0) 21.0 (18.0-24.0)
IQR 21.0, 23.0 19.0, 22.0
lar to the number who felt it was strictly disadvantageous; On the basis of open-field responses, major themes
however, substantially more students in the simulator group among stated advantages of simulator training by students
specifically felt that there were both advantages and dis- in the simulator group were the ability to visualize simu-
advantages associated with simulator training (9 students lated fundus lesions (10 [76.9%] of 13 respondents) and
[52.94%] vs 2 students [12.5%] in the traditional group, ability to practice without bothering a patient or classmate
P = .026, Fisher exact test). (4 respondents [30.8%]). Students in the traditional group
viewed lack of these factors as disadvantages while practic- of learning ophthalmoscopy. We identified better perfor-
ing on students with normal fundi or patients who might be mance among students in the simulator-trained group on
bothered by extended examinations. Major themes among 3 measures: independent practice time, technique (ability
stated disadvantages of simulator training by students in the to handle a direct ophthalmoscope and conduct an exami-
simulator group were the unrealistic training environment nation), and, based on the results of 1 patient examination,
(5 [38.4%] of 13 respondents), lack of experience in posi- the ability to locate fundus lesions accurately.
tioning relative to, and interacting with, a live person (3 Longer practice time among students in the simulator
respondents [23.1%]), and unfamiliarity with actual direct group is likely attributable to the novelty of the device and
ophthalmoscope controls before examination of patients the fact that students did not have to depend on others to
(8 respondents [61.5%]). Conversely, students in the tradi- practice. The exercises are engaging and the simulator pro-
tional group considered working with live individuals, using vides immediate feedback. One can hypothesize that longer
a real ophthalmoscope, to be an advantage. Lack of real- practice time will ultimately result in better skills, but prac-
time feedback was viewed as a disadvantage by 1 student in tice time alone did not explain better technique scores or
the traditional group. ability to localize lesions by the simulator group.
With regard to comfort in performing direct ophthal- With regard to technique, handling of the direct oph-
moscopy during assessments, no student in either train- thalmoscope was taught to both groups in the didactic ses-
ing group felt “very comfortable.” When training groups sion, but proper technique is reinforced by the simulator; for
were compared, more students in the simulator group felt example, correct positioning of the hand piece is required
“somewhat comfortable,” whereas more students in the tra- to view the simulated fundus. By mapping that portion of
ditional group felt “somewhat uncomfortable” or “not at all the fundus viewed by the operator, the simulator reinforced
comfortable,” although the differences were not statistically didactic instructions about how to scan the posterior pole
significant. efficiently, which might explain why the simulator group
was better able to identify the location of the lesion in 1
patient’s eye.
On a computerized literature search using PubMed, we
found only 1 previous study that investigated the effect
DISCUSSION of training on the Eyesi Direct Ophthalmoscope simula-
tor. Boden and associates12 randomized 34 German medical
Direct ophthalmoscopy is a difficult skill for many medical
students to “classic” and “simulator” training groups dur-
students to learn. This study sought to determine the effect
ing an ophthalmology rotation. All students received the
of a direct ophthalmoscope simulator on the early stages