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DEPARTMENT OF OPHTHALMOLOGY
KECK SCHOOL OF MEDICINE OF USC
40
YEARS
INSIGHT
DEPARTMENT OF OPHTHALMOLOGY
KECK SCHOOL OF MEDICINE OF USC
Keck School of Medicine of USC
Department of Ophthalmology
USC Eye Institute
1450 San Pablo Street
Los Angeles, CA 90033-4682
(800) USC-CARE
KeckMedicine.org
eye.usc.edu
©2015 Keck Medicine of USC
40
YEARS
INSIGHT
10
USC Eye Institute
TOP
ACCOLADES AND ACHIEVEMENTS
FOR 20 YEARS
Ophthalmology
U.S. News & World Report
2014-2015
• Ranked among the nation’s top 10 ophthalmology
programs for 20 years by U.S. News & World Report.
• Ranked among the nation’s top 10 ophthalmology
programs by Ophthalmology Times.
• Ranked in the top 10 for research funding by the National
Eye Institute.
• Headquarters of two California Institute of Regenerative
Medicine (CIRM) grants since 2012. USC leads the
development of a translational stem cell-based treatment
for age-related macular degeneration. CIRM funds stem cellbased research at institutions throughout California with the
goal of developing new therapies for diseases and disorders.
• Headquarters of the National Science Foundation
(NSF) Biomimetic MicroElectronic Systems Engineering
Research Center since 2003. USC leads an NSF-funded
national center for developing electronic devices that can
be implanted to treat diseases, conditions and injuries of
the eye.
• Headquarters of the Department of Energy (DOE)
Artificial Retina Project (2002-2012). USC leads a DOEfunded consortium whose goal is to develop a bioelectronic
retinal implant to restore sight to the blind.
INSIGHT
• António Champalimaud Vision Award in 2012 for
outstanding scientific research in the field of vision science
— Carmen A. Puliafito, MD, MBA, dean of the
Keck School of Medicine of USC.
2014 ANNUAL REPORT
•One of the nation’s top one percent of ophthalmologists in
2012 by U.S. News & World Report — Mark S. Humayun, MD, PhD.
• Top Doctors for 2014: USC ophthalmologists named
America’s Top Doctors - Los Angeles (Castle Connolly) 8;
Pasadena Magazine 11; Hollywood Reporter 8.
• 17 current United States ophthalmology chairs are former
faculty members and graduates of Keck School of Medicine
of USC Department of Ophthalmology training programs.
About the Cover:
Image of brain connectivity from the Human Connectome Project, led by USC. Research on
neural connections may help advance the development of new types of visual prostheses.
40 Years of Innovation
8
Patient Care
11
Research
16
Clinical Education 36
RETINITIS PIGMENTOSA CELLS
1
History has honed our skills and capabilities. This year, we celebrate 40 years of
life-changing research, compassionate care, and leadership in education.
The future inspires hard work and compassion. We envision a world where one of
humankind’s greatest fears — loss of vision — is a thing of the past.
How will we get there? With insights we have learned over four decades:
Insight in Research: An outside-the-box, innovative research program that tackles
the toughest of challenges — from diagnosing and treating imperiled eyesight in utero
to putting stem cells to work to solve age-related macular degeneration to building a
working artificial retina that will restore sight to the blind.
Insight in Patient Care: A commitment to taking care of people and to crafting the very
best solutions to the challenges our patients face. Good enough is never good enough.
Bench scientist, front-line physician, staff — we all collaborate across disciplines to
deliver the gift of sight.
Insight in Education: More than 400 young physicians applied for six spots in our
residency program. Our program is widely known as among the toughest in the country.
We attract the best, the brightest and the fiercely dedicated. No wonder that USC Eye
Institute thrives in supplying the world with the next generation of leaders.
After 40 years, these are our insights; and like true Trojans, we will fight on until we achieve
our mission: Vision for all. We invite you to join us. With your support and your advocacy,
we see a clear path to success.
“ Although the research, care and education we deliver is complex,
our mission is very simple. Our physicians and researchers come
to work every day with a single goal: to transform the lives of
people facing loss of vision or blindness.”
Sincerely,
Rohit Varma, MD, MPH
Grace and Emery Beardsley Professor
Chair, Department of Ophthalmology, Keck School of Medicine of USC
Director, USC Eye Institute
Rohit Varma. Director
(from left)
Carmen A. Puliafito,MD, MBA, Dean, Keck School of Medicine of USC
Rohit Varma, MD, MPH, Director, USC Eye Institute
Tom Jackiewicz, MPH, Senior Vice President and Chief Executive Officer, Keck Medicine of USC
2
3
Vision is Our Mission
PROTECTING
USC Eye Institute leads major research in the epidemiology of
eye disease to help prevent blindness.
PRESERVING
USC Eye Institute diagnoses, treats and manages the most
complex eye conditions, from in utero to advanced age.
RESTORING
USC Eye Institute integrates and applies emerging technologies
to develop new methods to restore sight to the blind.
Fulfillment of our mission is best expressed in the remarkable triumphs
of our patients. Read their stories in the pages ahead.
4
5
40 YEARS OF
INNOVATION
Major Breakthroughs by USC Department
of Ophthalmology Faculty
1974-2014
INSIGHT
40 Years of
Innovation
1974 Founded the USC Department of
Opthalmology
1978 Developed a laboratory model of penetrating
eye injuries that influences the management of
trauma in humans
Since its founding 40 years ago, the
Department of Ophthalmology of the
Keck School of Medicine of USC has
pioneered many discoveries that have
contribute to the advancement of vision
science and clinical ophthalmology.
1979 Developed a laboratory model of choroidal
neovascularization now widely used to study
pathogenesis and treatment of subretinal
neovascularization
1987 Implanted the first artificial cornea in a
pediatric patient
Our faculty has a long tradition of seeking
and sharing knowledge to help protect,
preserve and restore precious eyesight.
1987 Identified the gene that causes
retinoblastoma
In the pages that follow, we highlight
significant achievements by current and
former USC Department of Ophthalmology
faculty members.
1991 Pioneered optical coherence tomography
1992 Addressed vision complications from AIDS
by diagnosing and developing treatments for
opportunistic eye infections and Kaposi’s sarcoma
1998 Developed the Baerveldt® glaucoma implant
for preserving vision in glaucoma patients by
reducing eye pressure
1999 Developed a noninvasive glucose-monitoring
system using Raman spectrum signals from the
aqueous humor
2000 Began the Los Angeles Latino Eye Study,
the world’s largest investigation into eye disease
in Latinos
PIONEERING BREAKTHROUGHS, THEN AND NOW
Optical coherence tomography, pioneered by Carmen A. Puliafito, dean
of the Keck School of Medicine of USC, is an essential diagnostic tool used
worldwide.
Hyperspectral imaging, being developed by USC Eye Institute researchers,
is providing images of the retina that reveal its spectroscopic features in
unprecedented detail.
ARTIFICIAL RETINA IMPLANT
6
7
2002 Implanted the first artificial retina in a
patient after beginning collaboration with the U.S.
Department of Energy Office of Science in 1999
2014 Discovered which retinal cells mutate to
become retinoblastoma
2005 Pioneered use of ultra-high speed Fournier
domain optical coherence tomography (OCT) to
improve glaucoma diagnosis
INSIGHT
Patient
Care
2007 Implanted first Argus II Retinal Prosthesis
System in the United States
2009 Identified the unique mechanism of uptake
in lacrimal gland for adenovirus 5 that may
facilitate drug delivery
2010 Developed a Web-accessible visual field test
and analysis system for multicenter studies and
touchpad device access
2011 Began first clinical trials for an experimental
therapeutic agent to treat Leber’s Hereditary
Optic Neuropathy, a mitochondrial disease
2013 Received Argus II Retinal Prosthesis System
approval by the United States Food and Drug
Administration for patients with retinitis pigmentosa
In 2014, USC Eye Institute had the privilege
of treating many thousands of patients who
were facing the possibility of loss of vision
or blindness. People from all walks of life
with a full spectrum of eye conditions
relied on us to provide the most advanced
care possible.
The programmable micropump implanted by USC physicians
2014 Implanted a programmable micropump
smart device that delivers precise small doses
of medications into the eyes of patients with
diabetic macular edema, in the first-in-man
clinical trial
PIONEERING BREAKTHROUGHS, THEN AND NOW
The Baerveldt® glaucoma implant, developed at USC, has become the
global standard for glaucoma surgery.
8
The gel stent, developed by USC Eye Institute researchers, is implanted
through a minimally invasive injection and has been shown to reduce
intraocular pressure from glaucoma.
RETINAL STEM CELLS
9
Abe Spigner
Ocular Laceration,
Retinal Detachment
OCULAR HISTORY
3/16/14 Ocular laceration OS
resulting in open globe, traumatic
cataract and vitreous hemorrhage.
Presented with LP vision and at risk
for permanent blindness.
TREATMENT
•3/16/14 Primary closure surgery.
•3/18/14 Evaluation revealed
hyphema, traumatic cataract and
vitreous hemorrhage.
When a wine glass shattered and sent a shard slicing
into his left eye, Abe Spigner expected to lose his sight.
Abe was rushed to USC Verdugo Hills Hospital and then
transferred to LAC+USC Medical Center for primary surgical
repair of his eye. Two days later at the USC Eye Institute, retinal
specialist Lisa Olmos de Koo, MD, and cornea surgeon J. Martin
Heur, MD, PhD, planned and performed successful surgery to
save Abe’s left eye.
A month later, the vision in Abe’s left eye suddenly worsened and
he returned to the USC Eye Institute. Diagnosed with a retinal
detachment, he underwent surgery that included inserting a gas
bubble into his eye to hold the retina in place as it healed.
Required to remain face down for seven days following surgery
to keep the bubble in the proper position, Abe occupied himself
•3/31/14 Planned surgery: vitrectomy
and lensectomy and AC washout
by building a radio-controlled truck. In the process, he
•4/28/14 Sudden vision change. Diagnosed
with macula-sparing retinal detachment.
Detachment was repaired emergently
with scleral buckle, vitrectomy and gas
tamponade. Anterior wound revision was
performed concurrently.
from his childhood.
•Poor candidate for rigid gas permeable
and soft contact lenses due to severe dry
eye and irregular corneal shape.
Abe
contributed to a very positive outcome — and rekindled a hobby
In the months since surgery, Abe’s left eye has healed fully and he
now has 20/25 vision corrected vision.
J. Martin Heur, MD, PhD,
associate professor of clinical
ophthalmology, worked with retinal
specialist Lisa Olmos de Koo, MD, MBA,
assistant professor of ophthalmology, to
save Abe Spigner’s left eye.
OUTCOME
In preliminary tests with prosthetic
replacement of the ocular surface
ecosystem (PROSE) therapy, custom
scleral device improved vision to 20/25.
Left eye fundus taken approx. seven months
after detachment repair shows the retina
is attached and healthy. The 360-degree
indentation of the encircling buckle with laser
marks on the crest is evident. A small amount
of pre-retinal fibrosis superotemporal to the
disc is apparent, but clinically insignificant.
10
11
PATIENT CARE
Comprehensive Clinical Services
A full spectrum of highly specialized eye care for patients of all ages.
CORNEAL AND EXTERNAL DISEASES
Comprehensive corneal evaluations,
medical diagnostic services and
computerized topography can often
be performed during a single
visit. Available diagnostic services
include pachymetry, potential acuity
measurement, microbiological
studies and assessment of corneal
topography using computerized
corneal modeling technology.
GLAUCOMA
Targeted and Culturally Personalized Care
Linda Lam, MD, specializes in medical and surgical treatment of retinal diseases.
She also specializes in ensuring that the USC Eye Institute reaches patients where
they live and addresses their specific needs.
The composition of the team of specialists and subspecialists in
Arcadia reflects the residents’ greater susceptibility to myopia,
narrow angle glaucoma, cataracts, dry eye, diabetic retinopathy
and age-related macular degeneration.
OCULAR ONCOLOGY
Specialists provide a broad range of
diagnostic, medical and surgical services
with access to cancer specialists from
USC Norris Comprehensive Cancer
The team can also address patients fluently in Mandarin, Cantonese,
Vietnamese, Korean, Hindi, as well as Spanish and German.
To make it easier for patients to see eye specialists and keep their
appointments, the new clinic is located in the center of the city,
adjacent to a soon-to-be-built Metro station.
12
NEURO-OPHTHALMOLOGY, ORBITAL
AND ADULT STRABISMUS
Specializing in disorders of the
optic nerve, chronic papilledema
and orbital trauma, our physicians
provide consultations, and medical
and surgical services. Available
diagnostic testing includes fluorescein
angiography, ultrasonography, visual
fields and electrophysiology.
As medical director of the recently relocated and expanded
ophthalmology clinic in Arcadia, CA, Lam is attuned to the clinical
and cultural nuances of the predominantly Asian neighborhood .
Effective, personalized care is based on welcoming patients, meeting
their needs and removing barriers to care. The Arcadia location
expansion is the latest example of how the USC Eye Institute is
achieving this goal.
Glaucoma specialists provide comprehensive
consultative, diagnostic, medical and
surgical services. Faculty members are
involved in a National Eye Institute
sponsored, multicenter clinical trial studying
the efficacy and safety of early surgery in the
treatment of glaucoma.
Center as needed. We specialize in the
treatment of choroidal melanoma and
other ocular tumors in adults, treatment
of retinoblastoma and other ocular
tumors in children and new treatment
methodologies for intraocular tumors.
OPHTHALMIC PATHOLOGY
We provide macroscopic, microscopic
and ultrastructural analysis of diseased
eye tissues to aid in diagnosis. Advanced
genomic, proteomic and cytogenetic
techniques are also used to diagnose
diseases at a molecular level.
OPHTHALMIC PLASTICS, ORBITAL
AND RECONSTRUCTIVE SURGERY
Our physicians specialize in tissues
surrounding the eyeball that affect the
appearance or function of the eye. This
includes diseases of the eyelids, the
lacrimal system, the orbit and the facial
areas adjacent to the eye. Ophthalmic
plastic surgeons are board-certified
ophthalmologists who have completed
several years of additional, highly
specialized training in plastic surgery.
OPTOMETRY AND CORNEAL
PROSTHESIS
We have expertise in fitting specialty
contact lenses, and offer innovative
prosthetic replacement of the ocular
surface ecosystem (PROSE).
PEDIATRIC OPHTHALMOLOGY
A full range of diagnostic and treatment
methodologies are available through
USC Department of Ophthalmology Patient Volumes
Linda A. Lam, MD, associate professor of ophthalmology and vice
chair, satellite clinical affairs
Year
Total Visits
Total Surgeries
2013
95,000
4,700
2014
114,000
5,480
Totals include Keck Medicine of USC, Children’s Hospital Los Angeles, LAC+USC Medical Center
and VA Greater LA Healthcare System
Children’s Hospital Los Angeles, including
the ability to measure visual acuity in
infants and preverbal children. Our
specialists have expertise in diagnosis
and treatment of ocular oncology,
neuro-ophthalmology, retinal disorders
and strabismus.
REFRACTIVE SURGERY
We were one of the few ophthalmic
centers in the country involved in the
U.S. Food and Drug Administration
supervised clinical trial testing of
the efficacy of the excimer laser, and
continue to be at the forefront of
developments in refractive surgery.
UVEITIS AND OCULAR
INFLAMMATION
Our specialists evaluate the functional
status of the immune system and
detect infectious causes or neoplastic
processes. Electron microscopic and
immunohistochemical techniques often
lead to diagnosis of rare diseases. Highly
specialized services dealing with AIDSrelated cytomegalovirus (CMV) retinitis
are also available.
VITREORETINAL SURGERY AND
RETINAL DISEASE
We specialize in the repair of complex
retinal detachments, offering advanced
techniques such as silicone oil,
perfluorocarbon liquids and SF6 and
C3F8 gases. Our specialists have the
surgical and research experience to repair
penetrating trauma. Laser treatment of
the retina for diabetic retinopathy can be
performed with the argon, krypton, diode,
or double frequency YAG laser.
FOR REFERRING PHYSICIANS
To consult with an ophthalmologist
from the USC Eye Institute, or to
schedule appointments, please call
(323) 442-6335.
13
Ruby Chan
Bilateral Retinoblastoma
MEDICAL HISTORY
Premature birth. Diagnosed with
retinoblastoma before she was
barely term.
Ruby Chan was born prematurely and diagnosed with
cancer in both of her eyes. She began treatment at Children’s
Hospital Los Angeles with Jesse L. Berry, MD, USC Eye Institute
specialist in ocular oncology. Ruby’s parents, Michael and Nellie,
took Nellie for chemotherapy for the first four months after
diagnosis, and continue with appointments for laser therapy.
Ruby has made great progress. Both of Ruby’s eyes were saved,
and her left eye is expected to have good vision.
Germline mutation places her at
greater risk for cancers.
Ruby
OCULAR HISTORY
Bilateral retinoblastoma, the right eye
involves the macula.
TREATMENT
Chemotherapy and laser therapy every
3-4 weeks since birth.
OUTCOME
Both eyes saved from cancer. Near
Ruby’s family includes her parents, Michael and Nellie, and her older brother, Rock.
normal vision expected in the left eye.
Image of the right eye shows a central scar
involving the macula after laser consolidation
for group B retinoblastoma, and a new tumor
adjacent to the nerve.
14
Jesse L. Berry, MD, assistant professor
of clinical ophthalmology, and Jonathan
Kim, MD, associate professor of clinical
ophthalmology, often collaborate to treat
vision problems in young patients at
Children’s Hospital Los Angeles.
15
RESEARCH
INSIGHT
Research
USC Eye Institute clinician-scientists drive
fundamental and translational research
to advance patient care by establishing
relationships that foster innovation. Our
clinician-scientists conduct bench clinical
trials and train the next generation of
ophthalmologists at clinical locations where
patient-centered collaboration improves vision
and fuels the development of new therapies.
Delivering Precise Drug Therapy for
Retinal Disease
Effective treatment for eye diseases
often depends on adherence to a
carefully planned regimen of eye
drops. Unfortunately, many patients
are unable to stay on schedule or
provide the correct dosage.
Our research moves from patient to bench
to bedside to meet the real needs of patients
and enhance their lives.
To improve patient compliance,
researchers at USC Eye Institute
developed a “smart” device to control
medical dosing. A tiny, implantable
pump delivers precise amounts of
medication as required at proper
intervals directly into the eye. It is
refillable, and is programmed and
recharged wirelessly.
Originally developed for treating
glaucoma, the second-generation
micropump system is designed for
retinal disease. It is smaller, has a
greater reservoir volume and offers
the possibility of multiple chambers
for more than one medication. For
retinal patients, localized delivery
of medications into the eye has the
advantage of eliminating possible
systemic side effects.
In 2014, USC Eye Institute physicians
performed noninvasive surgery for
the first-in-man implant of the novel
ophthalmic medication-delivery
system in patients with diabetic
macular edema. The clinical trial is
to verify the device’s feasibility for
controlled drug delivery for chronic
diseases of the retina. Further
investigations will evaluate its
effectiveness and be used to fine-tune
its operation.
The micropump is practical and
convenient to use. The medication
reservoir can be refilled with up to
100 microliters within two minutes via
a thin 31-gauge needle. It stores up to
12 months of medication before
requiring a refill. The device has been
shown to function effectively for up to
seven years.
This second-generation micropump
holds the promise of delivering
microdoses of medication to an exact
schedule so patients with diabetic
macular edema experience optimal
outcomes from therapy — without
being concerned about putting drops
in their eyes.
The World Health Organization
estimates that only half of patients in
developed countries follow treatment
recommendations. This tiny pump has
the potential for a huge impact.
USC Eye Institute retinal specialists Mark
S. Humayun, MD, PhD, professor of
ophthalmology and biomedical engineering,
and Damien Rodger, MD, PhD, assistant
professor of clinical ophthalmology as of
August 2015 (current fellow), are leading the
development of the micropump.
NORMAL RETINAL CELLS
16
17
Sheila Papayans
Age-related Macular
Degeneration (AMD)
OCULAR HISTORY
Family history and long personal history
of dry AMD in both eyes. Presented
emergently after one day of distorted
vision of left eye. Diagnosed with early
wet macular degeneration of the left eye.
Sheila Papayans watched helplessly as AMD took away
her sister’s eyesight. Sheila had the same condition and was
anticipating the same outcome. Attuned to any changes in her
vision, Sheila noticed a sudden distortion in what she saw with
her left eye. Wasting no time, she came to the USC Eye Institute.
Lisa Olmos de Koo, MD, a retinal specialist, confirmed that Sheila
had early wet macular degeneration of the left eye and prescribed
a regimen of therapeutic injections. Sheila agreed to start that
very same day.
Treatment was highly successful, most likely because Sheila
TREATMENT
noticed symptoms early and responded immediately. Sheila also
Treated with intravitreal injections of
anti-Vascular Endothelial Growth Factor
therapy to her left eye (ranibizumab
then aflibercept). Initial treat and extend
protocol soon switched to therapy as
needed. Had eight injections in left eye
over approx. 2.5 years. Took Age-Related
Eye Disease study formula antioxidant eye
vitamins to reduce the chances that the
right eye would convert from dry to wet.
began taking age-related eye disease formula vitamins to reduce
Sheila
the risk of developing wet AMD in her right eye.
Two years later, Sheila has no further symptoms of wet AMD in
her left eye. Her right eye, highly susceptible to wet AMD, remains
dry. Now enjoying good vision in both eyes, Sheila remains vigilant
and grateful.
OUTCOME
Maintains excellent vision in both eyes,
despite developing a potentially blinding
retinal disease. Right eye has remained
dry. Annual therapy of three injections
per year is far below the national
average. Vision is currently 20/25 in
each eye.
Initial OCT image shows subtle findings of wet macular degeneration, confirmed by
subsequent fluorescein angiography.
Lisa Olmos de Koo, MD, MBA,
assistant professor of clinical
ophthalmology, specializes in
medical and surgical treatment
of complex retinal diseases. She
is also the primary investigator
on clinical trials for the Argus II
artificial retina.
18
19
RESEARCH
Currently Active Fundamental Research Funding:
Department of Ophthalmology, Keck School of Medicine
of USC
as of January 2015
PROJECT
SOURCE
PRINCIPAL INVESTIGATOR
Snapshot Retinal Imaging Mueller Matrix Polarimeter
NIH
Amir Kashani, MD, PhD
Molecular Remedy of Mitochondrial Defects
NIH
Biju Thomas, PhD
Restoring vision by sheet transplants of retinal progenitors and retinal
pigment epithelium (RPE) derived from human embryonic stem cells
(hESCs)
CIRM
Biju Thomas, PhD
An Experimental Approach to Masculopathy
NIH
David Hinton, PhD
Zebrafish Model of Human Corneal Development and Disease
NIH
J. Martin Heur, MD, PhD
Research to Prevent Blindness (RPB) Career Development Award
RPB
J. Martin Heur, MD, PhD
Experimental and Clinical Investigations of Retinal Stimulation
NIH
James Weiland, PhD
Novel Ultra-Flexible Hybrid Circuits for Intraocular Retinal Prostheses
NIH
James Weiland, PhD
U.S. Army
James Weiland, PhD
INSPIRE: Bioelectronic Systems for Investigating Neural Plasticity
NSF
James Weiland, PhD
EAGER: Neural Plasticity Driven by Electrical Stimulation of the Retina
NSF
James Weiland, PhD
Biocompatible Hermetic Coatings, High Density Feedthroughs, and
Hermeticity Test Chips for Implantable Biomedical Devices
DARPA
James Weiland, PhD
VRPI Thermoresponsive Reversibly Attachable Patch for Temporary
Intervention in Ocular Trauma
U.S. Army
Mark Humayun, MD, PhD
Harrington Discovery
Institute
Mark Humayun, MD, PhD
Retinal Nanophotoswitch
NSF
Mark Humayun, MD, PhD
Phase 1 Safety Assessment of CPCB-RPE1, hESC-derived RPE Cell Coated
Parylene Membrane Implants, in Patients with Advanced Dry Age-Related
Macular Degeneration
CIRM
Mark Humayun, MD, PhD
A Novel Treatment for Retinal Ischemia
NIH
Mark Humayun, MD, PhD
An Engineering Research Center for Biomimetic Microelectronic Systems
NSF
Mark Humayun, MD, PhD
Mexican–American Glaucoma Genetic Study
NIH
Rohit Varma, MD, MPH
Primary Open Angle African-American Glaucoma Genetics
NIH
Rohit Varma, MD, MPH
African–American Eye Disease Study
NIH
Rohit Varma, MD, MPH
Los Angeles Latino Eye Study
NIH
Rohit Varma, MD, MPH
Wearable Visual Aid as Treatment for TBI Associated Visual Dysfunction
A Novel Treatment for Major Blinding Diseases
20
A layer of hESC-derived polarized RPE stem cells grown on the supporting parylene membrane (white) is shown implanted in the subretinal space.
Implanting Stem Cells to
Overcome AMD
Researchers at the USC Eye Institute are working to restore vision to patients with
advanced age-related macular degeneration (AMD). By growing thin sheets of stem
cell-derived cells and surgically implanting them into the eye to replace diseased
tissue, they hope to restore the retina’s critical light-sensitive cells.
USC stem cell researchers identified a stem cell line that contains the
characteristics of normal adult retinal pigment epithelium (RPE) cells. USC
bioengineers developed a material that can act as a scaffold for RPE cells to allow
them to function normally. Their collaborative advancements will be at the center
of Phase I clinical trials expected to begin within one year.
Retinal-cell implants have the potential to improve the lives of an estimated 1.75
million people in the United States who have AMD — the leading cause of vision
loss and blindness among the elderly.
David Hinton, MD, associate dean for
vision science, and Mark Humayun,
MD, PhD, professor of ophthalmology
and bioengineering, are principal
investigators for a $19 million grant from
the California Institute for Regenerative
Medicine to develop a stem cell-based
treatment for AMD.
21
RESEARCH
DISCOVERING AMERICANS’ VISION RISKS
LATINOS
CHINESE-AMERICANS
Among Latinos with Type 2
A study is underway to obtain
diabetes, Native-American ancestry
prevalence estimates of visual
is a significant risk factor for
impairment, refractive error,
diabetic retinopathy, the leading
diabetic retinopathy, open-angle
cause of blindness in working-
and angle-closure glaucoma, lens
age adults in the United States,
opacities, and age-related macular
affecting more than 4 million
degeneration in Chinese-Americans.
Americans, age 40 and older.
CHILDREN
AFRICAN-AMERICANS
Myopia (nearsightedness) and
African-Americans bear a heavier
hyperopia (farsightedness) vary
burden of diabetic macular edema
widely among children of different
(DME), one of the leading causes
ethnic groups. For example,
of blindness in diabetic patients in
African-American children are
the United States. Although Latinos
most likely to have myopia but
have the highest incidence of
least likely to have hyperopia,
diabetes, more African-Americans
compared to Latino and non-
suffer from its vision complications.
Hispanic white children.
Major Studies of
Minority Populations
USC Eye Institute research about
the prevalence and impact of
eye diseases in many vulnerable
populations includes:
• Los Angeles Latino Eye Study
(LALES), 1999–2014
• Multi-Ethnic Pediatric Eye
Disease Study (MEPEDS),
2003-2011
• Chinese-American Eye Study
(CHES), 2008-2013
• African-American Eye Disease
Study (AFEDS), 2013-2018
Image of perifoveal region of a fetal-week 19 retina shows retinoblastoma suppressor protein
(stained in red) expressed at especially high levels in nuclei of cone precursors (stained in green).
Leukocoria, a white reflection from within
the eye, is often the first sign of a growing
retinoblastoma tumor.
Identifying the Cause of
Retinoblastoma
Retinoblastoma is an eye cancer that usually affects children one to two
years of age. Although rare, it is the most common malignant tumor of
the eye in children. Left untreated, retinoblastoma can be fatal or result
in blindness.
USC Eye Institute faculty researcher David E. Cobrinik, MD, PhD, and his
colleagues made a major breakthrough in 2014 by identifying the type of cell
and signaling pathways that lead to the development of retinoblastoma.
Protecting Vision through
Community Health Research
Through an ongoing series of comprehensive studies, principal investigator
USC Eye Institute epidemiologists
Xuejuan Jiang, PhD, assistant
professor of research, and Rohit Varma,
MD, MPH, professor and chair, USC
Department of Ophthalmology, lead
community health research.
Cobrinik’s research discovered that retinoblastomas originate in immature
cone photoreceptor cells that have not fully differentiated. When the RB1
gene in those cells mutates, it no longer encodes a tumor suppressor protein
(Rb) that prevents excessive cell growth, resulting in the development of
retinoblastoma tumors.
Rohit Varma, MD, MPH, director of the USC Eye Institute, is defining important
These findings significantly advance the understanding of cancer
differences in eye disease among various ethnic groups.
because they more generally imply that cancers can develop through
Many of the studies, the first of their kind ever conducted, are identifying
major risk factors. This new knowledge leads to improvements in vision care
and informs the government in setting effective goals for preventive eye
care and treatment.
the collaboration between a cancer-causing mutation — in this case,
inactivation of the RB1 gene — and the circuitry of the cell of origin that
sensitizes Rb protein loss.
Ultimately, Cobrinik and his research team aim to characterize the cell typespecific signaling pathways that collaborate with RB1 inactivation to identify
therapeutic targets for retinoblastoma and other cancers.
22
USC Eye Institute faculty involved in
retinoblastoma research include Alan
Linn Murphree, MD, (top left) who
identified the RB1 gene, David Cobrinik,
MD, PhD, (top right), Jonathan Kim,
MD, (bottom left) and Jesse Berry, MD,
(bottom right)
23
Harry Svoboda
Advanced Glaucoma
Harry Svoboda’s glaucoma went undiagnosed for many
years because it presented in just one eye and had not
caused any discomfort. When Harry’s right eye became
MEDICAL HISTORY
irritated consistently, she sought help and was finally was
Advanced primary open-angle glaucoma,
right eye. Unaffected left eye.
diagnosed with glaucoma.
Wanting the best of care, Harry drove more than two hours to the
OCULAR HISTORY
USC Eye Institute for an appointment with glaucoma-specialist
Elevated intraocular pressure to 40
mmHg in the right eye despite maximum
medical therapy including Diamox. No
evidence of ocular ischemic syndrome
(carotid duplex negative). No CNS
pathology. No evidence of trauma. No
inflammation or steroid use.
Alena Reznik, MD. Initially, Reznik prescribed a regimen of eye
drops. When that proved ineffective, she performed a specialized
procedure that included injection of an anti-scarring agent.
Harry’s eye pressure soon decreased to normal levels. Reznik
Harry
checks Harry’s eye pressures on a regular basis, so Harry can
continue to enjoy life to its fullest.
Glaucoma Under Control
Right Eye IOP: Harry Svoboda
TREATMENT
Trabeculectomy with subconjunctival
injection of Mitomycin-C prior to
surgery, resulting in less trauma and
greater diffusion.
DATE
PRESSURE
NOTES
8/15/14
39
Initial presentation
OUTCOME
9/12/14
24
All topical drops, oral Diamox
10/13/14
39
Despite all topical drops, unable
to tolerate Diamox
10/24/14
20
No drops/No Diamox
POD 1 after trabeculectomy with
subconjunctival injection of
Mitomycin C
11/17/14
12
No drops/No Diamox
Right eye IOP reduced from 39 to 12.
Alena Reznik, MD, assistant professor
of clinical ophthalmology, is a
glaucoma specialist.
24
25
RESEARCH
James D. Weiland, PhD, professor of ophthalmology and biomedical engineering, is deputy director of the Biometric MicroElectronic Systems
Engineering Center at USC.
TOP 10 PUBLICATIONS BY USC EYE INSTITUTE FACULTY PRIMARY INVESTIGATORS
David Cobrinik, MD, PhD
1. X
u XL, Singh HP, Wang L, Qi DL,
Poulos BK, Abramson DH, Jhanwar
SC, Cobrinik D. Rb suppresses human
cone-precursor-derived retinoblastoma
tumours. Nature. Oct 16, 2014;
514(7522):385-8.
Cheryl Craft, PhD
2. R
ebrik TI Botchkina I, Craft CM,
Korenbrot, JI. CNG-Modulin: the elusive
modulator of cone photoreceptor
cGMP-gated channel. Journal of
Neuroscience. Feb 29 2012;32(9):314253 and Cover.
Mark Humayun, MD, PhD and
James Weiland, PhD
3. N
anduri D, Horasager A, Boynton
G, Humayun MS, Greenberg RJ,
Weiland JD. Frequency and Amplitude
Modulation Have Different Effects on the
Percepts Elicited by Retinal Stimulation.
Invest Ophthalmol Vis Sci. Jan 20, 2012;
53 (1) 205-214.
4. W
eiland JD, Faraji B, Greenberg RJ,
Humayun MS, Shellock F. Assessment
of MRI issues for the Argus II retinal
prosthesis. Magn Reson Imaging.
Apr 30, 2012;3, 382-389.
Amir Kashani, MD, PhD
5. L opez-Jamie GR, Kashani AH, Saati S,
Martin G, Chader G, Humayun, MS.
Acute Variations in Retinal Vascular
Oxygen Content in a Rabbit Model of
Retinal Venous Occlusion. PLOS ONE.
Nov 6, 2012;7 (11), e50179.
Carmen A. Puliafito, MD, MBA
6. D
ai C, Liu X, Zhang HF, Puliafito CA,
Jiao S. Absolute retinal blood flow
measurement with a dual-beam
Doppler optical coherence tomography.
Invest Ophthalmol Vis Sci. Dec 9, 2013;
54(13):7998-8003.
Arthur Toga, PhD
7. N
ovak NM, Stein JL, Medland SE, Hibar
DP, Thompson PM, Toga AW. EnigmaVis:
Online interactive visualization of
The complete list of 2014 publications by USC Eye Institute faculty is on page 43.
26
genome-wide association studies of
the Enhancing NeuroImaging Genetics
through Meta-Analysis (ENIGMA)
Consortium. Twin Res Hum Genet. 2012;
15(3):414-8.
8. T oga AW, Clark KA, Thompson PM,
Shattuck DW, Van Horn JD. Mapping
the human connectome. Neurosurgery.
2012; 71(1):1-5.
Rohit Varma, MD, MPH
9. V
arma R, Bressler NM, Doan QV,
Gleeson M, Danese M, Bower JK, Selvin
E, Dolan C, Fine J, Colman S, Turpcu
A. Prevalence of and Risk Factor for
Diabetic Macular Edema in the United
States. JAMA Ophthalmol. 2014;
132(11):1334-1340.
10. Xie JZ, Tarczy-Hornoch K, Lin J, Cotter
SA, Torres M, Varma R. Color vision
deficiency in preschool children: the
multi-ethnic pediatric eye disease
study. Ophthalmology. July 2014;
121(7):1469-1474.
After implanting, the soft stent conforms to eye tissue and provides subconjuctival drainage of fluid.
Reinventing Glaucoma Treatment
For glaucoma patients who no longer
respond to medications or laser
trabeculoplasty, trabeculectomy and
tube shunt procedures are the most
effective treatments because they
rapidly lower intraocular pressure
(IOP). For decades, they have been
the most-performed glaucoma
surgeries worldwide.
Approximately the width of a human
hair, the stent is injected into the eye
through a small, self-sealing corneal
incision. It creates a gentle outflow of
fluid from the eye’s anterior chamber
into the surrounding subconjuctival
tissue. This pathway for drainage has
been proven effective and is preferred
by physicians worldwide.
Despite their proven effectiveness,
trabeculectomies and tube shunts
are highly invasive and have a oneyear complication rate as high as
50 percent for high-risk glaucoma
patients. Outcomes also have shown a
high degree of variability that can lead
to too little or too much IOP reduction.
Over time, shunts can become less
effective and require replacement.
The gel stent is pliable, noninflammatory and conforms to eye
tissue, which is likely to minimize
issues with migration, erosion and
corneal endothelial damage often
seen with synthetic materials.
The preloaded injector enables
standardized minimally invasive
insertion of the stent. International
clinical trials have shown that the gel
stent significantly and safely lowers
intraocular pressure.
Researchers at USC Eye Institute
have developed a more effective
alternative — a soft stent made of
permanent, collagen-derived gelatin.
The gel stent is approved in Europe
for primary open angle glaucoma
where other treatment methods
have failed. In the United States, it is
an investigational device, awaiting
approval by the U.S. Food and Drug
Administration.
This breakthrough holds the promise
to prevent glaucoma-related vision
loss through a broadly adoptable
10-minute procedure. Glaucoma is the
world’s No. 2 cause of blindness and
affects more than 60 million people
worldwide.
USC Eye Institute glaucoma specialists
Alena Reznik, MD, assistant professor
of clinical ophthalmology, and Rohit
Varma, MD, MPH, professor and chair,
Department of Ophthalmology, are
leading gel stent development.
27
Emily Mangel
Complex Corneal Disease
Emily
Emily Mangel was born with congenital varicella
syndrome, a rare disease that causes various
abnormalities of the body. For Emily, the disease affected her
MEDICAL HISTORY
right eye, right leg, and left arm and hand. Over many years of
Fetal varicella affected right eye, right
leg, and left arm/hand.
treatment at Children’s Hospital Los Angeles (CHLA), Emily made
tremendous progress in overcoming her challenges.
OCULAR HISTORY
For her right eye, Emily began treatment at age five with Mark
Keratoconjunctivitis sicca, neurotrophic
keratitis, perforated cornea, penetrating
keratoplasty and tarsorrhaphy.
specialists. Using medications, they preserved Emily’s corneal
Borchert, MD, and Jonathan Song, MD, USC Eye Institute corneal
surface from repeated thinning and healing until she reached her
early twenties, when multiple perforations led them to perform a
TREATMENT
Prosthetic replacement of the ocular
surface ecosystem (PROSE).
OUTCOME
Best corrected vision improved from
20/200 to 20/30 in the right eye with
PROSE device. Enhanced comfort and
ocular surface protection.
Emily began
treatment with
USC Eye Institute
specialists when
she was 5 years old,
shown here in a
Peter Pan costume
for Halloween.
corneal transplant. To protect the corneal surface, Emily’s right
eye was sewn shut for several months. When it was reopened, Emily’s
vision markedly improved.
To protect her corneal surface and further improve her vision, Emily
took advantage of an innovative treatment — prosthetic replacement
of the ocular surface ecosystem, or PROSE. Gloria Chiu, OD, fitted
Emily with the customized device and helped her learn how to
apply and remove it, despite limitations with her left hand. Emily
now wears the PROSE device on a daily basis and experiencing
improvements in eye comfort, vision and protection of the cornea.
The gas-permeable
PROSE device creates
a smooth optical
surface above the
cornea and bathes
the ocular surface
with a reservoir of
sterile saline.
A trio of USC Eye Institute specialists have provided 22 years of
continuous care for Emily’s complex vision challenges. Mark Borchert,
MD, (left), Gloria Chiu, OD, (center), Jonathan Song, MD, (right)
28
29
RESEARCH
Advancing Imaging of the Retina
Clinician-scientists at the USC Eye Institute, longtime innovators in ocular imaging, continue
to develop new technologies to advance diagnosis and treatment of eye disease.
Jeannie Chen, PhD, M. Elizabeth Fini, PhD, Scott Fraser PhD, and Sarah Hamm-Alvarez, PhD, are among the USC Eye Institute research collaborators
who published major papers in 2014.
TOP 10 PUBLICATIONS BY USC EYE INSTITUTE FACULTY COLLABORATORS
Jeannie Chen, PhD
1. M
oaven H, Koike Y, Jao C,
Gurevich VV, Langen R, Chen J.
Visual arrestin interactions with
clathrin adaptor AP2 regulates
photoreceptor cell survival. Proc Natl
Acad Sci. 2013; 110:9463-9468.
Scott Fraser, PhD
2. K
im DY, Finglera J, Zawadzki RJ, Park
SS, Morse LS, Schwartz DM, Fraser
SE, Werner JS. Optical imaging of the
chorioretinal vasculature in the living
human eye. Proc Natl Acad Sci. Aug 27,
2013;110(35); 14354-14359.
Elizabeth Fini, PhD
3. J eong S, Ledee DR, Gordon GM, Itakura
T, Patel N, Martin A, Quinn J, Fini ME.
Interaction of clusterin (CLU) and
matrix metalloproteinase-9 (MMP-9):
implications for epithelial homeostasis
and inflammation. American Journal of
Pathology. 2012;180:2028-39.
4. S antos ARC, Corredor RG, Obeso BA,
Wang Y, Trakhtenberg EF, Ponmattam
J, Dvoriantchikova G, Ivanov D,
Shestopalov VI, Goldberg JL, Fini
ME (co-senior author), Bajenaru ML.
Beta1 integrin-focal adhesion kinase
(FAK) signaling modulates retinal
ganglion cell survival. PLOS ONE, 2012,
7(10):e48332.
Sarah Hamm-Alvarez, PhD
5. X
u S, Ma L, Evans E, Okamoto
T, Hamm-Alvarez SF. Polymeric
immunoglobulin A receptor traffics
through two distinct apically-targeted
pathways in primary lacrimal gland
acinar cells. J Cell Sci. 2013;
126:2704-2717.
6. H
amm-Alvarez SF, Janga SR, EdmanWoolcott MC, Madrigal S, Shah M,
Frousiakis S, Renduchintala K, Zhu
J, Bricel S, Silka K, Bach D, Heur M,
Christianakis S, Arkfeld DA, Stohl
W. Tear Cathepsin S-A candidate
biomarker for Sjögren’s syndrome.
Arthritis Rheumatol. Jul 2014;
66(7):1872-81
Huizong Tao, PhD
7. L i YT, Ibrahim LA, Liu BH,
Zhang LI, Tao HW. Linear
transformation of thalamocortical
input by intracortical excitation. Nat
Neurosci. 2013;16:1324-1330.
The complete list of 2014 publications by USC Eye Institute faculty is on page 43.
30
Bosco S. Tjan, PhD
8. N
andy AS, Tjan BS. Saccadeconfounded image statistics explain
visual crowding. Nature Neuroscience.
2012;15(3), 463–469.
David Hinton, MD, PhD
9. S reekumar PG, Chothe P, Sharma KK,
Baid R, Kompella U, Spee C, Kannan N,
Manh C, Ryan SJ, Ganapathy V, Kannan
R, Hinton DR. Antiapoptotic properties
of alpha-crystallin-derived peptide
chaperones and characterization of
their uptake transporters in RPE
cells. Invest Ophthalmol Vis Sci. 2013;
54:2787-2798.
F eatured in the Investigative
Ophthalmology and Visual Science
Journal as “Research Highlight”:
Stern JH. Mini-Chaperones for Early
AMD. Invest Ophthalmol Vis Sci. 2013;
54:2799.
10.Zhou P, Kannan R, Spee C, Sreekumar
PG, Dou G, Hinton DR. Protection of
retina by aB crystallin in sodium iodate
induced retinal degeneration. PLOS
ONE. May, 29 2014;9(5):e98275.
OCT angiography image of the retina shows changes that occur in
diabetic retinopathy.
OCT angiography eliminates
need for dye injection
To assess the health of blood vessels
in the retina, physicians commonly use
fluorescein angiography — injecting
dye into a patient’s arm vein and taking
photographs of the eye with a special
camera that highlights the dye as it
circulates in the retinal vessels.
USC Eye Institute researchers are
eliminating the need for dye injections
when visualizing fine retinal capillaries
through advanced technology called
OCT angiography. This non-invasive
method works by isolating the reflected
light from the retina and identifying
the changes in the phase and intensity
of light that are associated with the
movement of blood.
Pre-clinical pilot studies show that
OCT angiography can reveal the
changes that occur in diseases such
Hyperspectral images from the camera built by the USC Eye Institute to
measure the oxygen levels inside the retinal vessels.
as diabetic retinopathy and retinal
vein occlusion much like fluorescein
angiography, but without the risk or
discomfort of any injection procedure.
Once FDA approved, it is likely that
OCT angiography will become an
important tool to help diagnose and
treat retinal diseases in the future.
Hyperspectral imaging
provides unprecedented detail
Through collaboration with optical
engineers and other scientists,
USC Eye Institute researchers have
built a camera that can measure the
spectroscopic features of the retina
in unprecedented detail. The camera
acquires images in seconds without
injections or other invasive procedures.
Using hyperspectral imaging,
studies demonstrated that patients
with advanced forms of diabetic
retinopathy have significant changes
in the amount of oxygen in the
retinal blood vessels. This may
suggest that the retina is not receiving
the appropriate amount of oxygen in
this disease.
The information available from
hyperspectral imaging holds
great promise for expanding the
understanding of retinopathy, retinal
vein occlusions, choroidal nevi and
melanoma, leading to advancements
in diagnosis and treatment.
Carmen A. Puliafito, MD, MBA, dean,
Keck School of Medicine, professor of
ophthalmology, and Amir Kashani,
MD, PhD, assistant professor of clinical
ophthalmology, are leading retinal imaging
research at the USC Eye Institute.
31
Margaret Hanopulus
Adult Strabismus
OCULAR HISTORY
Margaret Hanopulus was born with strabismus. The
alignment of her eyes was corrected with surgeries when
she was a toddler and a teenager. Since then, her eyes
gradually drifted out of alignment.
Infantile esotropia requiring previous
strabismus surgeries in 1958 and 1970.
After suffering a stroke and then successfully undergoing surgery
Developed large exotropia and
hypertropia over the years, with
significant deviation.
eye surgery was not as scary as she had previously thought.
TREATMENT
using an adjustable suture technique that enables exceptional
Exploration, resection of scar tissue and
advancement of previously recessed
medial recti (bilaterally) with adjustable
suture technique.
for an aneurysm, Margaret decided that having corrective
She consulted Vivek Patel, MD, a neuro-ophthalmology specialist
at the USC Eye Institute. Patel performed strabismus surgery
precision and long-term maintenance of correct position.
Margaret
Now Margaret’s eye alignment is the same as it was in her
teenage years.
OUTCOME
Pre-operative measurements of 35 PD XT
and 12 PD LHT improved to 4 PD ET and
no hypertropia. She does not experience
diplopia and will continue to improve
over time.
The adjustable suture technique affords remarkable precision and safety for
patients who have experienced multiple strabismus surgeries in the past.
Vivek Patel, MD, associate
professor of clinical
ophthalmology, is director
of neuro-ophthalmology
and adult strabismus at the
USC Eye Institute.
32
33
RESEARCH
USC Eye Institute Collaborators
To advance vision science and clinical ophthalmology, USC Eye Institute collaborates with many other research
organizations. We are grateful for their partnership and acknowledge their efforts in a variety of major initiatives.
INDIVIDUALS
Bioengineering Initiative
COLLABORATOR
Theodore Berger, PhD
Robert Chow, MD, PhD
Scott E. Fraser, PhD
Malancha Gupta, PhD
Hossein Hashemi, PhD
Laurent Itti, PhD
Gianluca Lazzi, PhD
Mark Liker, MD
Gerard Medioni, PhD
Ellis Meng, PhD
Alapakkam Sampath, PhD
Kirk Shung, PhD
Dong Song, PhD
Armand Tanguay, PhD
ORGANIZATION
USC (Biomedical Engineering)
USC (Zhilka Institute)
USC (Biomedical Engineering)
USC (Materials Science)
USC (Electrical Engineering)
USC (Computer Science)
University of Utah, UT
USC (Neurosurgery)
USC (Computer Science)
USC (Biomedical Engineering)
UCLA, CA
USC (Biomedical Engineering)
USC (Biomedical Engineering)
USC (Electrical Engineering)
Human Connectome Project
COLLABORATOR
James T. Becker, PhD
Adam L. Boxer, MD, PhD
Kyle Chard, PhD
Kristi Clark, PhD
Eric Deutsch, PhD
Ivo Dinov, PhD
James Duncan, PhD
Jerome Engel, MD
Ian Foster, PhD
Giovanni Frisoni, MD
Gustavo Glusman, PhD
Dana Goldman, PhD
Gerig Guido, PhD
Susan Hayflick, MD
Scott Holland, PhD
Leroy Hood, MD, PhD
John Van Horn, PhD
ORGANIZATION
University of Pittsburgh, PA
UCSF, CA
University of Chicago, IL
USC (Neurology)
Institute for Systems Biology, WA
University of Michigan, MI
Yale University, CT
UCLA, CA
University of Chicago, IL
IRCCS Fatebenefratelli, Italy
Institute for Systems Biology, WA
USC (Schaeffer Center for Health Policy
and Economics)
University of Utah, UT
Oregon Health & Science University, OR
Cincinnati Children’s
Research Foundation, OH
Institute for Systems Biology, WA
USC (Neurology)
COMPANIES
•Abbott Medical
Optics
•Advanced Bionics
•Alcon
•Allergan
•AqueSys
•Bausch & Lomb
•BioPhan
•Boston Scientific
•Carl Zeiss Meditech
•Cell Traffix
•Eli Lilly
•Genentech
•Harvest Precision
Technologies
34
Carl Kesselman, PhD
Richard Leahy, PhD
Robert Scott Mackin, PhD
Geoffrey T Manley, MD, PhD
Tom Nichols, PhD
Yuko Y. Palesch, PhD
Nathan Price, PhD
Bruce Rosen, MD, PhD
Howard Rosen, MD
Seth Seabury, PhD
Yonggang Shi, PhD
Olaf Sporns, PhD
Michael Weiner, MD
Wenle Zhao, PhD
USC (Industrial and Systems Engineering)
USC (Electrical Engineering)
UCSF, CA
UCSF, CA
University of Warwick, United Kingdom
Medical University of South Carolina, SC
Institute for Systems Biology, WA
Massachusetts General Hospital, MA
UCSF, CA
USC (Schaeffer Center for Health Policy
and Economics)
USC (Neurology)
Indiana University, IN
Northern California Institute for
Research & Education, CA
Medical University of South Carolina, SC
Imaging Initiative
COLLABORATOR
Antonio Capone, MD
Thomas Karnowski, PhD
Michael Trese, MD
George Williams, MD
Mark Wong, PhD
ORGANIZATION
Oakland University, MI
Oak Ridge National Labs, TN
Oakland University, MI
Oakland University, MI
National Aeronautics and Space
Administration, MD
Ocular Epidemiology
COLLABORATOR
Stanley Azen, PhD
Xiaoyi Gao, PhD
James Gauderman, PhD
Joanne Katz, ScD
Ronald Klein, MD, MPH
Roberta McKean-Cowdin, PhD
Joan M. O’Brien, MD
Jeremy Rotter, PhD
Kristina Tarczy-Hornoch, MD
Tien Wong, MD, PhD
ORGANIZATION
USC (Preventive Medicine)
University of Illinois at Chicago, IL
USC (Preventive Medicine)
Johns Hopkins University, MD
University of Wisconsin-Madison, WI
USC (Preventive Medicine)
University of Pennsylvania, PA
Los Angeles Biomedical Institute, CA
Seattle Children's Hospital, WA
National University of Singapore, Singapore
USC EYE INSTITUTE COLLABORATORS
•Iridex
•MCNC
•Medtronic
•Morgan Technical
Ceramics
•NOCO
•Nanodynamics
•National
Semiconductor
•OProbe
•Premitec
•Product
Development
Technologies
•Quallion
•Reichert Technologies
•Replenish Inc.
•Santen, Inc.
•Second Sight
•St. Jude ANS
•Stryker
•SurModics
•Synergetics
•Texas Instruments
•Ventrex
•Virginia Technologies
09% U.S. Research
Institutions within California
46% U.S. Research
Institutions outside California
04% International Research
Institutions
41% University of
Southern California:
Other Departments
Argus II is comprised of an eyeglass-mounted camera that sends signals
to an implanted 60-electrode receiver, which transmits them to the
retina. Signals travel the optic nerve to the brain where they can be
interpreted as a visual picture.
During months of follow-up testing, Lisa will train her brain to see in a
new way, interpreting the signals sent by Argus II.
Fulfilling the Promise of Sight for the Blind
The world’s first retinal prosthesis
reached another milestone in 2014.
Lisa Kulik, blinded by retinitis
pigmentosa, became the first person
on the West Coast to be implanted
with the recently FDA-approved
Argus II.® Lisa Olmos de Koo, MD,
MBA, performed the four-hour
procedure at the Keck Medical
Center of USC.
On the first day of activation, Lisa
was already ahead of expectations
as she was able to see spots of light.
At a 4th of July celebration, she was
thrilled to see the light and movement
of fireworks. Progress continues as
Lisa learns to interpret the signals
sent by Argus ll. Confident that her
participation in Argus II research is
leading toward a cure for blindness,
Lisa also participates in a study to
determine whether partial restoration
of vision has an impact on how
the brain processes information.
She returns to USC periodically for
magnetic imaging resonance
(MRI) tests, as well as testing with
the Argus II.
Retinitis pigmentosa is a genetic
disease affecting nearly 100,000
people in the United States. As
the disease progresses, patients
experience night blindness, tunnel
vision, blurring and difficulty adjusting
from dark to light environments.
Eventually their vision is reduced
to shadows and most victims are
declared legally blind. For these
patients, the improvement of vision
provided by Argus II would be nothing
short of a miracle.
USC Eye Institute retinal specialists
Lisa Olmos de Koo, MD, MBA, assistant
professor of clinical ophthalmology, and
Mark Humayun, MD, PhD, professor of
ophthalmology and bioengineering, are
leading further development of Argus II.
35
CLINICAL EDUCATION
Exceptional Clinical Education
The USC Eye Institute provides a residency and fellowship training experience with
unique clinical and research opportunities.
INSIGHT
Clinical
Education
Clinical education is one of the defining
principles at the USC Eye Institute.
Visiting professor Joseph Miller, MD, MPH, professor and head, Ophthalmology and Vision Science from the
University of Arizona College of Medicine, lectures residents.
Our tradition of academic excellence in
training leading clinicians and researchers in
ophthalmology is well documented. Among
current United States ophthalmology chairs,
17 are former faculty members and graduates
of Keck School of Medicine of USC Department
of Ophthalmology training programs.
Priority is on training, mentoring
and inspiring future leaders in four
diverse and highly acute clinical and
surgical settings:
· USC Eye Institute at Keck Medical
Center of USC, ranked as a top 10
program by U.S. News & World
Report for 20 years
The USC Eye Institute is proud to be training
the next generation of leaders.
· Children’s Hospital Los Angeles
(CHLA), ranked among the top five
children’s hospitals in the U.S.
· Los Angeles County (LAC) + USC
Medical Center, one of nation’s
largest public hospitals
· VA Greater Los Angeles Healthcare
System, serving the needs of
generations of veterans.
As one of the most funded eye
institutes in the world, the USC
Eye Institute collaborates across
CORNEAL ENDOTHELIUM CELLS
36
disciplines with a wide variety of
industries and institutions. It is an
ideal interdisciplinary environment
for physicians who have a passion to
be an important part of internationally
recognized, cutting-edge vision science.
Medical Education
Keck School of Medicine of USC
has 27 basic science and academic
departments with more than 1,500
full-time faculty members. Future
physicians receive comprehensive
training from an ophthalmology
faculty that has been ranked in the
top 10 nationally by U.S. News &
World Report for 20 years.
USC Eye Institute faculty who oversee
clinical ophthalmology education, from top
left, include Malvin Anders, MD, chief of
ophthalmology, LAC+USC Medical Center;
Jesse Berry, MD, associate residency
program director; Vivek Patel, MD,
residency program director; Neda Shamie,
MD, director of medical education; Rohit
Varma, MD, MPH; chair, department of
ophthalmology; and Carmen A. Puliafito,
MD, MBA, dean, Keck School of Medicine,
professor of ophthalmology.
37
Stan Bard
Uveitis
OCULAR HISTORY
Referred for two weeks of uveitis
of unclear etiology, found to have
Without warning, both of Stan Bard’s eyes suddenly
became red and his vision began to blur. He thought
the problem was temporary irritation that would go away, but it
became worse. Stan consulted several eye specialists, but none
was able to offer lasting relief. He became increasingly alarmed
when he could neither focus on objects at arm’s length, nor read.
a multifocal serpiginoid pattern of
After two weeks, Stan’s search for an answer led him to the USC
chorioretinal inflammation in both
Eye Institute. He consulted with Narsing Rao, MD, Director of
eyes thought to be of herpetic origin.
the Ophthalmic Pathology Laboratory and Uveitis Service, and
TREATMENT
Treated with antivirals with dramatic
improvement in two days then started
Damien Rodger, MD, PhD. The uveitis specialists made a thorough
evaluation and decided on a treatment plan that included
antiviral medications, followed by a course of oral steroids.
on oral steroids.
Upon treatment, Stan’s eyes showed marked improvement within
OUTCOME
its normal state: 20/25 in his right eye and 20/20 in his left eye.
Vision improved from 20/70 to 20/25
in the right eye and 20/100 to 20/20 in
the left eye.
Stan
several days. The redness disappeared and his vision returned to
UPON PRESENTATION
AFTER TWO DAYS OF TREATMENT
Widefield fundus images of the right and left eyes below show the dramatic resolution
of uveitis.
Narsing Rao, MD, professor of
ophthalmology and pathology, and Damien
Rodger, MD, PhD, a vitreoretinal surgery
fellow who will become an assistant
professor in 2015, worked together to restore
Stan’s vision.
38
39
CLINICAL EDUCATION
USC Eye Institute Full-time Faculty,
Residents and Fellows 2014-15
Faculty, Fellows and Residents
Residents
Each year, the USC Eye Institute recruits exceptional residents. The incoming six residents for 2014-15 were accepted from
more than 400 applicants.
3RD YEAR
Lloyd Cuzzo, MD
Co-Chief Resident
Tova Mannis, MD
Co-Chief Resident
Sahar Bedrood,
MD, PhD
Andrew Browne,
MD, PhD
Yohko Murakami, MD
Saloomeh Saati, MD
Mica Bergman,
MD, PhD
Lilangi
Ediriwickrema,
MD, MS
Esther Lee Kim, MD
Sun Young Lee,
MD, PhD
Benjamin Xu,
MD, PhD
Dagny Zhu, MD
Jiun L. Do, MD, PhD
Stavros Moysidis, MD
Billy Pan, MD
Kelly Rue, MD
Grace Shih, MD
Philip Storey,
MD, MPH
Hossein Ameri, MD
Vitreoretinal
Surgery
Meena George, MD
Vitreoretinal
Surgery
Daniel Greene, MD
Cornea & External
Disease
Luxme Hariharan
MD, MPH, Pediatric
Cornea, Cataract &
Glaucoma
Hossein Nazari, MD
Medical Retina
Grace Richter,
MD, MPH
Damien Rodger,
MD, PhD
Vitreoretinal Surgery
Namita Sagar, MD
Glaucoma
Hangxiu Xu, MD, PhD
Neuro-ophthalmology
2ND YEAR
1ST YEAR
Fellows and Clinical Instructors
The USC Eye Institute offers clinical fellowship
training in six subspecialty areas, including
cornea and external disease, glaucoma, neoophthalmology, ophthalmic plastic surgery,
retina and uveitis.
Informal research fellowships are also
awarded by each service and laboratory
independently. USC attracts promising
academic ophthalmologists from around the
world who spend one or two years participating
in research programs. Many return to their
home countries where they assume positions
of national or international leadership.
40
41
CLINICAL EDUCATION
USC Eye Institute Full-time Faculty
Secondary, Tertiary and Joint Appointment Faculty
Hossein Ameri, MD
Assistant Professor
(as of July 2015)
Malvin Anders, MD
Associate Professor
Jesse Berry, MD
Assistant Professor
Mark Borchert, MD
Professor
Angela Buffenn,
MD, MPH
Assistant Professor
Gloria Chiu, OD
Assistant Professor
David Cobrinik, PhD
Associate Professor
•
•
•
•
•
•
Joseph Cocozza,
Assistant Professor
J eannie Chen, PhD, Cell & Neurobiology
M. Elizabeth Fini, PhD, Cell & Neurobiology
Sarah Hamm-Alvarez, PhD, Pharmacology
Shikun He, MD, Pathology
David Hinton, MD, Pathology
Florence Hofman, PhD, Pathology
•Eun Jin Lee, PhD, Biomedical Engineering
•Austin K. Mircheff, PhD, Physiology
•Maria E. Sibug Saber, MD, Pathology
•Joel E. Schechter, PhD, Cell & Neurobiology
•Huizhong W. Tao, PhD, Cell & Neurobiology
USC Collaborating Faculty
• S cott Fraser, PhD, Biomedical Engineering
• Judith Hirsch, PhD, Neurobiology
• Aaron McGee, PhD, Pediatrics
• Bosco Tjan, PhD, Psychology
Biju Thomas, PhD, assistant professor of clinical ophthalmology
Cheryl Craft, PhD
Professor
Charles Flowers,MD
Associate Professor
Henry Fong, PhD
Associate Professor
J. Martin Heur,
MD, PhD
Associate Professor
Mark Humayun,
MD, PhD
Professor
Veronica Isozaki, OD
Assistant Professor
Shunwu Jeong, PhD
Assistant Professor
Xuejuan Jiang, PhD
Assistant Professor
2014 Publications
1. Cheung AY, Kashani AH, Drenser KA. Subretinal
peripapillary neovascularization associated
with persistent fetal vasculature. Retin Cases
Brief Rep. 2014 Winter;8(1):83-6
Amir Kashani,
MD, PhD
Assistant Professor
Jonathan Kim, MD
Associate Professor
Linda Lam, MD
Associate Professor
Carlos Lastra, MD
Clinical Instructor
Thomas Lee, MD
Associate Professor
Debbie Mitra, PhD
Assistant Professor
Andrew Moshfeghi,
MD
Associate Professor
Arlanna Moshfeghi,
MD, MBA
Assistant Professor
2. Wu DM, Fawzi AA, Recasens MA, Bertoni
B, Chopra V, Rao NA, Eliott D. Good visual
outcome after repair of a very large macular
hole with neurosensory retinal operculum.
Retin Cases Brief Rep. 2014 Spring;8(2):138-40
3. Samimi DB, Chiu GB, Burnstine MA. Prose
scleral lens: A novel aid for staged eyelid
reconstruction. Ophthal Plast Reconstr Surg.
2014 Sep-Oct;30(5):e119-21
4. Ameri H. Retinal prosthesis, potential future
approaches. Clin Experiment Ophthalmol. 2014
Sep-Oct;42(7):599-600
Alan Linn
Murphree, MD
Professor
Grace Richter,
MD, MPH
Assistant Professor
(as of Aug 2015)
Rohit Varma, MD,
MPH, Professor
42
Sudha Nallasamy,MD
Assistant Professor
Damien Rodger,
MD, PhD
Assistant Professor
(as of Aug 2015)
Dandan Wang, MD
Clinical Instructor
Lisa Olmos de Koo,
MD, MBA
Assistant Professor
Neda Shamie, MD
Associate Professor
James Weiland, PhD
Professor
Vivek Patel, MD
Associate Professor
Jonathan Song, MD
Associate Professor
Andrew Weitz, PhD
Assistant Professor
Carmen Puliafito,
MD, MBA
Professor
Biju Thomas, PhD
Assistant Professor
John Whalen, PhD
Assistant Professor
Narsing Rao, MD
Professor
Paul Thompson,
PhD, Professor
Sandy ZhangNunes, MD
Assistant Professor
Bibiana Reiser, MD
Assistant Professor
Arthur Toga, PhD
Provost Professor
Alena Reznik, MD
Assistant Professor
Lernik Torossian, OD
Assistant Professor
5. Valenzuela F, Browne A, Srur M, Nieme C,
Zanolli M, Lopez-Solis R, Traipe L. Combined
phacoemulsification and ahmed glaucoma
drainage implant surgery for patients with
refractory glaucoma and cataract. J Glaucoma.
2014 Sep 26
6. Saeed S, Quintin J, Kerstens HH, Rao NA,
Aghajanirefah A, Matarese F, Cheng SC, Ratter
J, Berentsen K, van der Ent MA, Sharifi N,
Janssen-Megens EM, Ter Huurne M, Mandoli
A, van Schaik T, Ng A, Burden F, Downes K,
Frontini M, Kumar V, Giamarellos-Bourboulis
EJ, Ouwehand WH, van der Meer JW, Joosten
LA, Wijmenga C, Martens JH, Xavier RJ, Logie
C, Netea MG, Stunnenberg HG. Epigenetic
programming of monocyte-to-macrophage
differentiation and trained innate immunity.
Science. 2014 Sep 26;345(6204):1251086
7. Cheng SC, Quintin J, Cramer RA, Shepardson
KM, Saeed S, Kumar V, Giamarellos-Bourboulis
EJ, Martens JH, Rao NA, Aghajanirefah A,
Manjeri GR, Li Y, Ifrim DC, Arts RJ, van der Meer
BM, Deen PM, Logie C, O’Neill LA, Willems P,
van de Veerdonk FL, van der Meer JW, Ng A,
Joosten LA, Wijmenga C, Stunnenberg HG,
Xavier RJ, Netea MG. Mtor- and hif-1alphamediated aerobic glycolysis as metabolic
basis for trained immunity. Science. 2014 Sep
26;345(6204):1250684
8. Zhang-Nunes SX, Dang S, Garneau HC,
Hwang C, Isaacs D, Chang SH, Goldberg R.
Characterization and outcomes of repeat
orbital decompression for thyroid-associated
orbitopathy. Orbit. 2014 Sep 22:1-9
9. Babiloni C, Del Percio C, Boccardi M, Lizio
R, Lopez S, Carducci F, Marzano N, Soricelli
A, Ferri R, Triggiani AI, Prestia A, Salinari S,
Rasser PE, Basar E, Fama F, Nobili F, Yener G,
Emek-Savas DD, Loreto G, Mundi C, Thompson
PM, Rossini PM, Frisoni GB. Occipital sources of
resting-state alpha rhythms are related to local
gray matter density in subjects with amnesic
mild cognitive impairment and alzheimer’s
disease. Neurobiol Aging. 2014 Sep 21
10. Lee JG, Heur M. Interleukin-1beta-induced
wnt5a enhances human corneal endothelial
cell migration through regulation of cdc42 and
rhoa. Mol Cell Biol. 2014 Sep 15;34(18):3535-45
11. Riverol M, Becker JT, Lopez OL, Raji CA,
Thompson PM, Carmichael OT, Gach HM,
Longstreth Jr WT, Fried L, Tracy RP, Kuller LH.
Relationship between systemic and cerebral
vascular disease and brain structure integrity
in normal elderly individuals. J Alzheimers Dis.
2014 Sep 11
12. Narendra DP, Wang N, Erkkinen MG,
Jagadeesan J, Lee TC, Zimmerman EE, Klein JP.
An anomalous developmental venous anomaly.
Neurology. 2014 Sep 9;83(11):1033-4
13. Puliafito CA. Oct angiography: The next era
of oct technology emerges. Ophthalmic Surg
Lasers Imaging Retina. 2014 Sep 1;45(5):360
14. Adogwa O, Huang MI, Thompson PM,
Darlington T, Cheng JS, Gokaslan ZL, Gottfried
ON, Bagley CA, Anderson GD, Isaacs RE. No
difference in postoperative complications,
pain, and functional outcomes up to 2 years
after incidental durotomy in lumbar spinal
fusion: A prospective, multi-institutional,
propensity-matched analysis of 1,741 patients.
Spine J. 2014 Sep 1;14(9):1828-34
15. Thomas JB, Brier MR, Bateman RJ, Snyder AZ,
Benzinger TL, Xiong C, Raichle M, Holtzman
DM, Sperling RA, Mayeux R, Ghetti B, Ringman
JM, Salloway S, McDade E, Rossor MN,
Ourselin S, Schofield PR, Masters CL, Martins
RN, Weiner MW, Thompson PM, Fox NC,
Koeppe RA, Jack CR, Jr., Mathis CA, Oliver A,
Blazey TM, Moulder K, Buckles V, Hornbeck R,
Chhatwal J, Schultz AP, Goate AM, Fagan AM,
Cairns NJ, Marcus DS, Morris JC, Ances BM.
Functional connectivity in autosomal dominant
and late-onset alzheimer disease. JAMA
Neurol. 2014 Sep;71(9):1111-22
16. Khan MA, DeCroos FC, Storey PP, Shields JA,
Garg SJ, Shields CL. Outcomes of anti-vascular
endothelial growth factor therapy in the
management of choroidal neovascularization
associated with choroidal osteoma. Retina.
2014 Sep;34(9):1750-6
17. Kashani AH, Lopez Jaime GR, Saati S, Martin
G, Varma R, Humayun MS. Noninvasive
assessment of retinal vascular oxygen content
among normal and diabetic human subjects:
A study using hyperspectral computed
tomographic imaging spectroscopy. Retina.
2014 Sep;34(9):1854-60
18. Gao X, Gauderman WJ, Marjoram P, Torres
M, Chen YD, Taylor KD, Rotter JI, Varma R.
Native american ancestry is associated with
severe diabetic retinopathy in latinos. Invest
Ophthalmol Vis Sci. 2014 Sep;55(9):6041-5
19. Cavedo E, Pievani M, Boccardi M, Galluzzi S,
Bocchetta M, Bonetti M, Thompson PM, Frisoni
GB. Medial temporal atrophy in early and lateonset alzheimer’s disease. Neurobiol Aging.
2014 Sep;35(9):2004-12
20.Prasad G, Joshi AA, Feng A, Toga AW,
Thompson PM, Terzopoulos D. Skull-stripping
with machine learning deformable organisms. J
Neurosci Methods. 2014 Oct 30;236:114-24
43
CLINICAL EDUCATION
21. Xu XL, Singh HP, Wang L, Qi DL, Poulos BK,
Abramson DH, Jhanwar SC, Cobrinik D. Rb
suppresses human cone-precursor-derived
retinoblastoma tumours. Nature. 2014 Oct
16;514(7522):385-8
22. Shen KK, Rose S, Fripp J, McMahon KL, de
Zubicaray GI, Martin NG, Thompson PM,
Wright MJ, Salvado O. Investigating brain
connectivity heritability in a twin study using
diffusion imaging data. Neuroimage. 2014 Oct
15;100:628-41
23. Jin Y, Shi Y, Zhan L, Gutman BA, de Zubicaray
GI, McMahon KL, Wright MJ, Toga AW,
Thompson PM. Automatic clustering of white
matter fibers in brain diffusion mri with an
application to genetics. Neuroimage. 2014 Oct
15;100:75-90
24. Hill RH, 3rd, Czyz CN, Kandapalli S, ZhangNunes SX, Cahill KV, Wulc AE, Foster JA.
Evolving minimally invasive techniques for tear
trough enhancement. Ophthal Plast Reconstr
Surg. 2014 Oct 8
25. Ching CR, Hua X, Hibar DP, Ward CP, Gunter
JL, Bernstein MA, Jack CR, Jr., Weiner MW,
Thompson PM. Does mri scan acceleration
affect power to track brain change? Neurobiol
Aging. 2014 Oct 7
26. Storey P, Alshareef R, Khuthaila M, London
N, Leiby B, DeCroos C, Kaiser R. Pars plana
vitrectomy and scleral buckle versus pars
plana vitrectomy alone for patients with
rhegmatogenous retinal detachment at high
risk for proliferative vitreoretinopathy. Retina.
2014 Oct;34(10):1945-51
27. Raji CA, Erickson KI, Lopez OL, Kuller LH,
Gach HM, Thompson PM, Riverol M, Becker
JT. Regular fish consumption and age-related
brain gray matter loss. Am J Prev Med. 2014
Oct;47(4):444-51
28. Pan BX, Yee KM, Ross-Cisneros FN, Sadun
AA, Sebag J. Inner retinal optic neuropathy:
Vitreomacular surgery-associated disruption
of the inner retina. Invest Ophthalmol Vis Sci.
2014 Oct;55(10):6756-64
29. Xiang S, Yuan L, Fan W, Wang Y, Thompson
PM, Ye J. Bi-level multi-source learning for
heterogeneous block-wise missing data.
Neuroimage. 2014 Nov 15;102p1:192-206
30.Dennis EL, Jahanshad N, Braskie MN, Warstadt
NM, Hibar DP, Kohannim O, Nir TM, McMahon
KL, de Zubicaray GI, Montgomery GW, Martin
NG, Toga AW, Wright MJ, Thompson PM.
Obesity gene negr1 associated with white
matter integrity in healthy young adults.
Neuroimage. 2014 Nov 15;102 Pt 2:548-57
31. Couvy-Duchesne B, Blokland GA, Hickie IB,
Thompson PM, Martin NG, de Zubicaray GI,
McMahon KL, Wright MJ. Heritability of head
motion during resting state functional mri
in 462 healthy twins. Neuroimage. 2014 Nov
15;102 Pt 2:424-34
32. Patel VR, Zee DS. The cerebellum in eye
movement control: Nystagmus, coordinate
44
frames and disconjugacy. Eye (Lond). 2014
Nov 14
33. Tai AX, Song JC. Surgical outcomes of
baerveldt implants in pediatric glaucoma
patients. J aapos. 2014 Nov 12
34. Cunningham SI, Weiland JD, Bao P, LopezJaime GR, Tjan BS. Correlation of vision loss
with tactile-evoked v1 responses in retinitis
pigmentosa. Vision Res. 2014 Nov 3
35. Matsunaga D, Yi J, Puliafito CA, Kashani AH.
Oct angiography in healthy human subjects.
Ophthalmic Surg Lasers Imaging Retina. 2014
Nov 1;45(6):510-5
36. Warstadt NM, Dennis EL, Jahanshad N,
Kohannim O, Nir TM, McMahon KL, de
Zubicaray GI, Montgomery GW, Henders AK,
Martin NG, Whitfield JB, Jack CR, Jr., Bernstein
MA, Weiner MW, Toga AW, Wright MJ,
Thompson PM. Serum cholesterol and variant
in cholesterol-related gene cetp predict white
matter microstructure. Neurobiol Aging. 2014
Nov;35(11):2504-13
37. Varma R, Bressler NM, Doan QV, Gleeson M,
Danese M, Bower JK, Selvin E, Dolan C, Fine
J, Colman S, Turpcu A. Prevalence of and
risk factors for diabetic macular edema in
the united states. JAMA Ophthalmol. 2014
Nov;132(11):1334-40
38. Renteria ME, Hansell NK, Strike LT, McMahon
KL, de Zubicaray GI, Hickie IB, Thompson
PM, Martin NG, Medland SE, Wright MJ.
Genetic architecture of subcortical brain
regions: Common and region-specific genetic
contributions. Genes Brain Behav. 2014
Nov;13(8):821-30
39. Mah FS, Davidson R, Holland EJ, Hovanesian
J, John T, Kanellopoulos J, Shamie N, Starr
C, Vroman D, Kim T. Current knowledge about
and recommendations for ocular methicillinresistant staphylococcus aureus. J Cataract
Refract Surg. 2014 Nov;40(11):1894-908
40.40.Kashani AH, Brown KT, Chang E, Drenser
KA, Capone A, Trese MT. Diversity of retinal
vascular anomalies in patients with familial
exudative vitreoretinopathy. Ophthalmology.
2014 Nov;121(11):2220-7
41. Nugent AK, Paulus YM, Chan A, Kim JW,
Schwartz EJ, Moshfeghi DM. Multiple
myeloma recurrence with optic nerve
infiltration diagnosed by vitrectomy,
immunohistochemistry, and in situ
hybridization. Eur J Ophthalmol. 2014 MayJun;24(3):446-8
42. Roussotte FF, Gutman BA, Madsen SK, Colby
JB, Thompson PM. Combined effects of
alzheimer risk variants in the clu and apoe
genes on ventricular expansion patterns in the
elderly. J Neurosci. 2014 May 7;34(19):6537-45
45. Prasad G, Joshi SH, Thompson PM. Optimizing
brain connectivity networks for disease
classification using epic. Proc IEEE Int Symp
Biomed Imaging. 2014 May;2014:834-7
46. Pirotta E, Brookes KL, Graham IM, Thompson
PM. Variation in harbour porpoise activity in
response to seismic survey noise. Biol Lett.
2014 May;10(5):20131090
47. Hurtz S, Woo E, Kebets V, Green AE, Zoumalan
C, Wang B, Ringman JM, Thompson PM,
Apostolova LG. Age effects on cortical
thickness in cognitively normal elderly
individuals. Dement Geriatr Cogn Dis Extra.
2014 May;4(2):221-7
48. Gadelkarim JJ, Ajilore O, Schonfeld D, Zhan
L, Thompson PM, Feusner JD, Kumar A,
Altshuler LL, Leow AD. Investigating brain
community structure abnormalities in
bipolar disorder using path length associated
community estimation. Hum Brain Mapp. 2014
May;35(5):2253-64
49.Cannon TD, Sun F, McEwen SJ, Papademetris
X, He G, van Erp TG, Jacobson A, Bearden
CE, Walker E, Hu X, Zhou L, Seidman LJ,
Thermenos HW, Cornblatt B, Olvet DM,
Perkins D, Belger A, Cadenhead K, Tsuang
M, Mirzakhanian H, Addington J, Frayne R,
Woods SW, McGlashan TH, Constable RT,
Qiu M, Mathalon DH, Thompson P, Toga AW.
Reliability of neuroanatomical measurements
in a multisite longitudinal study of youth at
risk for psychosis. Hum Brain Mapp. 2014
May;35(5):2424-34
50. Borchert M, Garcia-Filion P, Fink C, Geffner
M, Nelson M. Re: Ramakrishnaiah et al.:
Reliability of magnetic resonance imaging for
the detection of hypopituitarism in children
with optic nerve hypoplasia (ophthalmology
2014;121:387-91). Ophthalmology. 2014
May;121(5):e26-7
51. Roussotte FF, Jahanshad N, Hibar DP,
Thompson PM. Altered regional brain volumes
in elderly carriers of a risk variant for drug
abuse in the dopamine d2 receptor gene
(drd2). Brain Imaging Behav. 2014 Mar 16
52. Yehoshua Z, de Amorim Garcia Filho CA, Nunes
RP, Gregori G, Penha FM, Moshfeghi AA, Zhang
K, Sadda S, Feuer W, Rosenfeld PJ. Systemic
complement inhibition with eculizumab
for geographic atrophy in age-related
macular degeneration: The complete study.
Ophthalmology. 2014 Mar;121(3):693-701
53. Wang M, Lu AT, Varma R, Schuman JS,
Greenfield DS, Huang D. Combining information
from 3 anatomic regions in the diagnosis of
glaucoma with time-domain optical coherence
tomography. J Glaucoma. 2014 Mar;23(3):129-35
43. Wong SC, Lee TC, Heier JS, Ho AC. Endoscopic
vitrectomy. Curr Opin Ophthalmol. 2014
May;25(3):195-206
54. Nir TM, Jahanshad N, Busovaca E, Wendelken
L, Nicolas K, Thompson PM, Valcour VG.
Mapping white matter integrity in elderly
people with hiv. Hum Brain Mapp. 2014
Mar;35(3):975-92
44.Weiland JD, Humayun MS. Retinal prosthesis.
IEEE Trans Biomed Eng. 2014 May;61(5):1412-24
55. Haas BW, Sheau K, Kelley RG, Thompson PM,
Reiss AL. Regionally specific increased volume
of the amygdala in williams syndrome: Evidence
from surface-based modeling. Hum Brain Mapp.
2014 Mar;35(3):866-74
56. Dennis EL, Thompson PM. Functional brain
connectivity using fmri in aging and alzheimer’s
disease. Neuropsychol Rev. 2014 Mar;24(1):49-62
57. Chen K, Weiland JD. Discovery of retinal
elastin and its possible role in age-related
macular degeneration. Ann Biomed Eng. 2014
Mar;42(3):678-84
58. Weiner MW, Veitch DP, Hayes J, Neylan T,
Grafman J, Aisen PS, Petersen RC, Jack C, Jagust
W, Trojanowski JQ, Shaw LM, Saykin AJ, Green
RC, Harvey D, Toga AW, Friedl KE, Pacifico
A, Sheline Y, Yaffe K, Mohlenoff B. Effects of
traumatic brain injury and posttraumatic stress
disorder on alzheimer’s disease in veterans,
using the alzheimer’s disease neuroimaging
initiative. Alzheimers Dement. 2014 Jun;10(3
Suppl):S226-35
59. Van Horn JD, Toga AW. Human neuroimaging as
a “big data” science. Brain Imaging Behav. 2014
Jun;8(2):323-31
60.Thompson PM, Stein JL, Medland SE, Hibar DP,
Vasquez AA, Renteria ME, Toro R, Jahanshad N,
Schumann G, Franke B, Wright MJ, Martin NG,
Agartz I, Alda M, Alhusaini S, Almasy L, Almeida
J, Alpert K, Andreasen NC, Andreassen OA,
Apostolova LG, Appel K, Armstrong NJ, Aribisala
B, Bastin ME, Bauer M, Bearden CE, Bergmann
O, Binder EB, Blangero J, Bockholt HJ, Boen
E, Bois C, Boomsma DI, Booth T, Bowman IJ,
Bralten J, Brouwer RM, Brunner HG, Brohawn
DG, Buckner RL, Buitelaar J, Bulayeva K, Bustillo
JR, Calhoun VD, Cannon DM, Cantor RM, Carless
MA, Caseras X, Cavalleri GL, Chakravarty MM,
Chang KD, Ching CR, Christoforou A, Cichon S,
Clark VP, Conrod P, Coppola G, Crespo-Facorro
B, Curran JE, Czisch M, Deary IJ, de Geus EJ,
den Braber A, Delvecchio G, Depondt C, de
Haan L, de Zubicaray GI, Dima D, Dimitrova R,
Djurovic S, Dong H, Donohoe G, Duggirala R,
Dyer TD, Ehrlich S, Ekman CJ, Elvsashagen T,
Emsell L, Erk S, Espeseth T, Fagerness J, Fears
S, Fedko I, Fernandez G, Fisher SE, Foroud T,
Fox PT, Francks C, Frangou S, Frey EM, Frodl T,
Frouin V, Garavan H, Giddaluru S, Glahn DC,
Godlewska B, Goldstein RZ, Gollub RL, Grabe
HJ, Grimm O, Gruber O, Guadalupe T, Gur
RE, Gur RC, Goring HH, Hagenaars S, Hajek
T, Hall GB, Hall J, Hardy J, Hartman CA, Hass
J, Hatton SN, Haukvik UK, Hegenscheid K,
Heinz A, Hickie IB, Ho BC, Hoehn D, Hoekstra
PJ, Hollinshead M, Holmes AJ, Homuth G,
Hoogman M, Hong LE, Hosten N, Hottenga
JJ, Hulshoff Pol HE, Hwang KS, Jack CR, Jr.,
Jenkinson M, Johnston C, Jonsson EG, Kahn
RS, Kasperaviciute D, Kelly S, Kim S, Kochunov
P, Koenders L, Kramer B, Kwok JB, Lagopoulos
J, Laje G, Landen M, Landman BA, Lauriello J,
Lawrie SM, Lee PH, Le Hellard S, Lemaitre H,
Leonardo CD, Li CS, Liberg B, Liewald DC, Liu
X, Lopez LM, Loth E, Lourdusamy A, Luciano
M, Macciardi F, Machielsen MW, Macqueen
GM, Malt UF, Mandl R, Manoach DS, Martinot
JL, Matarin M, Mather KA, Mattheisen M,
Mattingsdal M, Meyer-Lindenberg A, McDonald
C, McIntosh AM, McMahon FJ, McMahon KL,
Meisenzahl E, Melle I, Milaneschi Y, Mohnke
S, Montgomery GW, Morris DW, Moses EK,
Mueller BA, Munoz Maniega S, Muhleisen TW,
Muller-Myhsok B, Mwangi B, Nauck M, Nho K,
Nichols TE, Nilsson LG, Nugent AC, Nyberg L,
Olvera RL, Oosterlaan J, Ophoff RA, Pandolfo
M, Papalampropoulou-Tsiridou M, Papmeyer
M, Paus T, Pausova Z, Pearlson GD, Penninx
BW, Peterson CP, Pfennig A, Phillips M, Pike
GB, Poline JB, Potkin SG, Putz B, Ramasamy A,
Rasmussen J, Rietschel M, Rijpkema M, Risacher
SL, Roffman JL, Roiz-Santianez R, RomanczukSeiferth N, Rose EJ, Royle NA, Rujescu D,
Ryten M, Sachdev PS, Salami A, Satterthwaite
TD, Savitz J, Saykin AJ, Scanlon C, Schmaal L,
Schnack HG, Schork AJ, Schulz SC, Schur R,
Seidman L, Shen L, Shoemaker JM, Simmons A,
Sisodiya SM, Smith C, Smoller JW, Soares JC,
Sponheim SR, Sprooten E, Starr JM, Steen VM,
Strakowski S, Strike L, Sussmann J, Samann PG,
Teumer A, Toga AW, Tordesillas-Gutierrez D,
Trabzuni D, Trost S, Turner J, Van den Heuvel
M, van der Wee NJ, van Eijk K, van Erp TG,
van Haren NE, van ‘t Ent D, van Tol MJ, Valdes
Hernandez MC, Veltman DJ, Versace A, Volzke
H, Walker R, Walter H, Wang L, Wardlaw JM,
Weale ME, Weiner MW, Wen W, Westlye LT,
Whalley HC, Whelan CD, White T, Winkler AM,
Wittfeld K, Woldehawariat G, Wolf C, Zilles D,
Zwiers MP, Thalamuthu A, Schofield PR, Freimer
NB, Lawrence NS, Drevets W. The enigma
consortium: Large-scale collaborative analyses
of neuroimaging and genetic data. Brain Imaging
Behav. 2014 Jun;8(2):153-82
61. Shen L, Thompson PM, Potkin SG, Bertram
L, Farrer LA, Foroud TM, Green RC, Hu X,
Huentelman MJ, Kim S, Kauwe JS, Li Q, Liu
E, Macciardi F, Moore JH, Munsie L, Nho
K, Ramanan VK, Risacher SL, Stone DJ,
Swaminathan S, Toga AW, Weiner MW, Saykin AJ.
Genetic analysis of quantitative phenotypes in
ad and mci: Imaging, cognition and biomarkers.
Brain Imaging Behav. 2014 Jun;8(2):183-207
62. Roussotte FF, Gutman BA, Madsen SK, Colby
JB, Narr KL, Thompson PM. The apolipoprotein
e epsilon 4 allele is associated with ventricular
expansion rate and surface morphology in
dementia and normal aging. Neurobiol Aging.
2014 Jun;35(6):1309-17
63. Roussotte FF, Daianu M, Jahanshad N, Leonardo
CD, Thompson PM. Neuroimaging and genetic
risk for alzheimer’s disease and addictionrelated degenerative brain disorders. Brain
Imaging Behav. 2014 Jun;8(2):217-33
64. Peng DX, Kelley RG, Quintin EM, Raman M,
Thompson PM, Reiss AL. Cognitive and
behavioral correlates of caudate subregion
shape variation in fragile x syndrome. Hum Brain
Mapp. 2014 Jun;35(6):2861-8
65. Pefkianaki M, Westcott M, Liew G, Lee R, Pavesio
C, Rao NA, Gupta A, Bansal R, Khairallah
M, Kahloun R. Diagnostic and therapeutic
challenges. Retina. 2014 Jun;34(6):1247-52
66.Nazari H, Karakousis PC, Rao NA. Replication
of mycobacterium tuberculosis in retinal
pigment epithelium. JAMA Ophthalmol. 2014
Jun;132(6):724-9
67. Medland SE, Jahanshad N, Neale BM, Thompson
PM. Whole-genome analyses of whole-brain
data: Working within an expanded search space.
Nat Neurosci. 2014 Jun;17(6):791-800
68.Dinov ID, Petrosyan P, Liu Z, Eggert P, Zamanyan
A, Torri F, Macciardi F, Hobel S, Moon SW, Sung
YH, Jiang Z, Labus J, Kurth F, Ashe-McNalley C,
Mayer E, Vespa PM, Van Horn JD, Toga AW. The
perfect neuroimaging-genetics-computation
storm: Collision of petabytes of data, millions
of hardware devices and thousands of software
tools. Brain Imaging Behav. 2014 Jun;8(2):311-22
69.Chen K, Rowley AP, Weiland JD, Humayun MS.
Elastic properties of human posterior eye. J
Biomed Mater Res A. 2014 Jun;102(6):2001-7
70. Nicholson LB, Kim BT, Jardon J, TownsendPico W, Santos C, Moshfeghi AA, Albini TA,
Eliott D, Sobrin L. Severe bilateral ischemic
retinal vasculitis following cataract surgery.
Ophthalmic Surg Lasers Imaging Retina. 2014
Jul-Aug;45(4):338-42
71. Kashani AH, Cheung AY, Robinson J, Williams
GA. Longitudinal optical density analysis
of subretinal fluid after surgical repair of
rhegmatogenous retinal detachment. Retina.
2014 Jul 30
72. Braskie MN, Boyle CP, Rajagopalan P, Gutman
BA, Toga AW, Raji CA, Tracy RP, Kuller LH,
Becker JT, Lopez OL, Thompson PM. Physical
activity, inflammation, and volume of the aging
brain. Neuroscience. 2014 Jul 25;273:199-209
73. Kochunov P, Jahanshad N, Sprooten E, Nichols
TE, Mandl RC, Almasy L, Booth T, Brouwer
RM, Curran JE, de Zubicaray GI, Dimitrova R,
Duggirala R, Fox PT, Elliot Hong L, Landman BA,
Lemaitre H, Lopez LM, Martin NG, McMahon KL,
Mitchell BD, Olvera RL, Peterson CP, Starr JM,
Sussmann JE, Toga AW, Wardlaw JM, Wright MJ,
Wright SN, Bastin ME, McIntosh AM, Boomsma
DI, Kahn RS, den Braber A, de Geus EJ, Deary
IJ, Hulshoff Pol HE, Williamson DE, Blangero J,
van ‘t Ent D, Thompson PM, Glahn DC. Multi-site
study of additive genetic effects on fractional
anisotropy of cerebral white matter: Comparing
meta and megaanalytical approaches for data
pooling. Neuroimage. 2014 Jul 15;95:136-50
74. West SK, Moncada J, Munoz B, Mkocha H,
Storey P, Hardick J, Gaydos CA, Quinn TC,
Schachter J. Is there evidence for resistance of
ocular chlamydia trachomatis to azithromycin
after mass treatment for trachoma control? J
Infect Dis. 2014 Jul 1;210(1):65-71
75. Schwarz CG, Reid RI, Gunter JL, Senjem ML,
Przybelski SA, Zuk SM, Whitwell JL, Vemuri P,
Josephs KA, Kantarci K, Thompson PM, Petersen
RC, Jack CR, Jr. Improved dti registration allows
voxel-based analysis that outperforms tractbased spatial statistics. Neuroimage. 2014 Jul
1;94:65-78
45
CLINICAL EDUCATION
76. Guillaume B, Hua X, Thompson PM, Waldorp
L, Nichols TE. Fast and accurate modelling
of longitudinal and repeated measures
neuroimaging data. Neuroimage. 2014 Jul
1;94:287-302
77. Xie JZ, Tarczy-Hornoch K, Lin J, Cotter SA, Torres
M, Varma R. Color vision deficiency in preschool
children: The multi-ethnic pediatric eye disease
study. Ophthalmology. 2014 Jul;121(7):1469-74
78. Shi Y, Lai R, Wang DJ, Pelletier D, Mohr D,
Sicotte N, Toga AW. Metric optimization
for surface analysis in the laplace-beltrami
embedding space. IEEE Trans Med Imaging. 2014
Jul;33(7):1447-63
79. Nguyen P, Rue K, Heur M, Yiu SC. Ocular
surface rehabilitation: Application of human
amniotic membrane in high-risk penetrating
keratoplasties. Saudi J Ophthalmol. 2014
Jul;28(3):198-202
80.Heur M, Bach D, Theophanous C, Chiu GB.
Prosthetic replacement of the ocular surface
ecosystem scleral lens therapy for patients with
ocular symptoms of chronic stevens-johnson
syndrome. Am J Ophthalmol. 2014 Jul;158(1):49-54
81. Hamm-Alvarez SF, Janga SR, Edman MC,
Madrigal S, Shah M, Frousiakis SE, Renduchintala
K, Zhu J, Bricel S, Silka K, Bach D, Heur M,
Christianakis S, Arkfeld DG, Irvine J, Mack
WJ, Stohl W. Tear cathepsin s as a candidate
biomarker for sjogren’s syndrome. Arthritis
Rheumatol. 2014 Jul;66(7):1872-81
82. Chiu GB, Bach D, Theophanous C, Heur M.
Prosthetic replacement of the ocular surface
ecosystem (prose) scleral lens for salzmann’s
nodular degeneration. Saudi J Ophthalmol. 2014
Jul;28(3):203-6
83. Garcia Filho CA, Yehoshua Z, Gregori G, Nunes
RP, Penha FM, Moshfeghi AA, Zhang K, Feuer
W, Rosenfeld PJ. Change in drusen volume as
a novel clinical trial endpoint for the study of
complement inhibition in age-related macular
degeneration. Ophthalmic Surg Lasers Imaging
Retina. 2014 Jan-Feb;45(1):18-31
84.Cabrera M, Gonzalez A, Albini TA, Rowaan C,
Aguilar M, Lee W, Fortun JA, Moshfeghi AA,
Flynn HW, Jr., Parel JM. Differential flow rate
of commercially available triamcinolone with
and without preservative through small-gauge
needles. Ophthalmic Surg Lasers Imaging
Retina. 2014 Jan-Feb;45(1):54-7
85. Prestia A, Cavedo E, Boccardi M, Muscio C,
Adorni A, Geroldi C, Bonetti M, Thompson PM,
Frisoni GB. Hippocampal and amygdalar local
structural differences in elderly patients with
schizophrenia. Am J Geriatr Psychiatry. 2014 Jan 22
86.Merchant ND, Pirotta E, Barton TR, Thompson
PM. Monitoring ship noise to assess the impact
of coastal developments on marine mammals.
Mar Pollut Bull. 2014 Jan 15;78(1-2):85-95
87. Luders E, s Thompson PM. Why size matters:
Differences in brain volume account for
apparent sex differences in callosal anatomy:
The sexual dimorphism of the corpus callosum.
Neuroimage. 2014 Jan 1;84:820-4
46
88. Williams ME, Fink C, Zamora I, Borchert M.
Autism assessment in children with optic nerve
hypoplasia and other vision impairments. Dev
Med Child Neurol. 2014 Jan;56(1):66-72
89.Storey P, Dollin M, Pitcher J, Reddy S,
Vojtko J, Vander J, Hsu J, Garg SJ. The role
of topical antibiotic prophylaxis to prevent
endophthalmitis after intravitreal injection.
Ophthalmology. 2014 Jan;121(1):283-9
90.Labus JS, Dinov ID, Jiang Z, Ashe-McNalley C,
Zamanyan A, Shi Y, Hong JY, Gupta A, Tillisch
K, Ebrat B, Hobel S, Gutman BA, Joshi S,
Thompson PM, Toga AW, Mayer EA. Irritable
bowel syndrome in female patients is associated
with alterations in structural brain networks.
Pain. 2014 Jan;155(1):137-49
91. Kashani AH, Learned D, Nudleman E, Drenser
KA, Capone A, Trese MT. High prevalence of
peripheral retinal vascular anomalies in family
members of patients with familial exudative
vitreoretinopathy. Ophthalmology. 2014
Jan;121(1):262-8
92. He M, Abdou A, Ellwein LB, Naidoo KS, Sapkota
YD, Thulasiraj RD, Varma R, Zhao J, Kocur I,
Congdon NG. Age-related prevalence and met
need for correctable and uncorrectable near
vision impairment in a multi-country study.
Ophthalmology. 2014 Jan;121(1):417-22
93. Dean DC, 3rd, Jerskey BA, Chen K, Protas H,
Thiyyagura P, Roontiva A, O’Muircheartaigh J,
Dirks H, Waskiewicz N, Lehman K, Siniard AL,
Turk MN, Hua X, Madsen SK, Thompson PM,
Fleisher AS, Huentelman MJ, Deoni SC, Reiman
EM. Brain differences in infants at differential
genetic risk for late-onset alzheimer disease:
A cross-sectional imaging study. JAMA Neurol.
2014 Jan;71(1):11-22
94.Browne AW, Osher RH. Optimizing precision in
toric lens selection by combining keratometry
techniques. J Refract Surg. 2014 Jan;30(1):67-72
95. Zingg B, Hintiryan H, Gou L, Song MY, Bay M,
Bienkowski MS, Foster NN, Yamashita S,
Bowman I, Toga AW, Dong HW. Neural networks
of the mouse neocortex. Cell. 2014 Feb
27;156(5):1096-111
96.Looi JC, Velakoulis D, Walterfang M, GeorgiouKaristianis N, Macfarlane MD, Power BD, Nilsson
C, Styner M, Thompson PM, Van Westen D,
Wilkes FA, Wahlund LO. The australian, us,
scandinavian imaging exchange (aussie): An
innovative, virtually-integrated health research
network embedded in health care. Australas
Psychiatry. 2014 Feb 19;22(3):260-5
97. Dubey R, Zhou J, Wang Y, Thompson PM, Ye J.
Analysis of sampling techniques for imbalanced
data: An n = 648 adni study. Neuroimage. 2014
Feb 15;87:220-41
98.Blokland GA, McMahon KL, Thompson PM,
Hickie IB, Martin NG, de Zubicaray GI, Wright
MJ. Genetic effects on the cerebellar role in
working memory: Same brain, different genes?
Neuroimage. 2014 Feb 1;86:392-403
99.Weitz AC, Behrend MR, Ahuja AK, Christopher
P, Wei J, Wuyyuru V, Patel U, Greenberg
RJ, Humayun MS, Chow RH, Weiland JD.
Interphase gap as a means to reduce electrical
stimulation thresholds for epiretinal prostheses.
J Neural Eng. 2014 Feb;11(1):016007
109.Kim JW, Ngai LK, Sadda S, Murakami Y, Lee DK,
Murphree AL. Retcam fluorescein angiography
findings in eyes with advanced retinoblastoma.
Br J Ophthalmol. 2014 Dec;98(12):1666-71
100.Shan ZY, Wright MJ, Thompson PM, McMahon
KL, Blokland GG, de Zubicaray GI, Martin
NG, Vinkhuyzen AA, Reutens DC. Modeling of
the hemodynamic responses in block design
fmri studies. J Cereb Blood Flow Metab. 2014
Feb;34(2):316-24
110.Kempen JH, Sugar EA, Varma R, Dunn JP,
Heinemann MH, Jabs DA, Lyon AT, Lewis RA.
Risk of cataract among subjects with acquired
immune deficiency syndrome free of ocular
opportunistic infections. Ophthalmology. 2014
Dec;121(12):2317-24
101.Dennis EL, Thompson PM. Reprint of: Mapping
connectivity in the developing brain. Int J Dev
Neurosci. 2014 Feb;32:41-57
111.Clark KA, Helland T, Specht K, Narr KL, Manis
FR, Toga AW, Hugdahl K. Neuroanatomical
precursors of dyslexia identified from prereading through to age 11. Brain. 2014 Dec;137(Pt
12):3136-41
102.Cetingul HE, Wright MJ, Thompson PM, Vidal
R. Segmentation of high angular resolution
diffusion mri using sparse riemannian manifold
clustering. IEEE Trans Med Imaging. 2014
Feb;33(2):301-17
103.Bressler NM, Varma R, Doan QV, Gleeson M,
Danese M, Bower JK, Selvin E, Dolan C, Fine J,
Colman S, Turpcu A. Underuse of the health care
system by persons with diabetes mellitus and
diabetic macular edema in the united states.
JAMA Ophthalmol. 2014 Feb;132(2):168-73
112.Bressler NM, Varma R, Suner IJ, Dolan CM,
Ward J, Ehrlich JS, Colman S, Turpcu A. Visionrelated function after ranibizumab treatment for
diabetic macular edema: Results from ride and
rise. Ophthalmology. 2014 Dec;121(12):2461-72
113.Prasad G, Joshi SH, Nir TM, Toga AW, Thompson
PM. Brain connectivity and novel network
measures for alzheimer’s disease classification.
Neurobiol Aging. 2014 Aug 30
104.Ameri H, Liu H, Liu R, Ha Y, Paulucci-Holthauzen
AA, Hu S, Motamedi M, Godley BF, Tilton
RG, Zhang W. Tweak/fn14 pathway is a novel
mediator of retinal neovascularization. Invest
Ophthalmol Vis Sci. 2014 Feb;55(2):801-13
114.Nir TM, Jahanshad N, Toga AW, Bernstein
MA, Jack CR, Jr., Weiner MW, Thompson
PM. Connectivity network measures predict
volumetric atrophy in mild cognitive impairment.
Neurobiol Aging. 2014 Aug 30
105.Lam LA, Rodger DC. Bilateral macular
detachments, venous stasis retinopathy, and
retinal hemorrhages as initial presentation of
multiple myeloma: A case report. Retin Cases
Brief Rep. 2014 Fall;8(4):240-4
115.Madsen SK, Rajagopalan P, Joshi SH, Toga
AW, Thompson PM. Higher homocysteine
associated with thinner cortical gray matter in
803 participants from the alzheimer’s disease
neuroimaging initiative. Neurobiol Aging.
2014 Aug 30
106.Chalavi S, Vissia EM, Giesen ME, Nijenhuis ER,
Draijer N, Cole JH, Dazzan P, Pariante CM,
Madsen SK, Rajagopalan P, Thompson PM,
Toga AW, Veltman DJ, Reinders AA. Abnormal
hippocampal morphology in dissociative identity
disorder and post-traumatic stress disorder
correlates with childhood trauma and dissociative
symptoms. Hum Brain Mapp. 2014 Dec 29
107.Palmer ND, Goodarzi MO, Langefeld CD, Wang
N, Guo X, Taylor KD, Fingerlin TE, Norris JM,
Buchanan TA, Xiang AH, Haritunians T, Ziegler
JT, Williams AH, Stefansovski D, Cui J, Mackay
AW, Henkin LF, Bergman RN, Gao X, Gauderman
J, Varma R, Hanis CL, Cox NJ, Highland HM,
Below JE, Williams AL, Burtt NP, Aguilar-Salinas
CA, Huerta-Chagoya A, Gonzalez-Villalpando
C, Orozco L, Haiman CA, Tsai MY, Johnson WC,
Yao J, Rasmussen-Torvik L, Pankow J, Snively
B, Jackson RD, Liu S, Nadler JL, Kandeel F,
Chen YI, Bowden DW, Rich SS, Raffel LJ, Rotter
JI, Watanabe RM, Wagenknecht LE. Genetic
variants associated with quantitative glucose
homeostasis traits translate to type 2 diabetes
in mexican americans: The guardian (genetics
underlying diabetes in hispanics) consortium.
Diabetes. 2014 Dec 18
108.Toga AW, Thompson PM. Connectopathy in ageing
and dementia. Brain. 2014 Dec;137(Pt 12):3104-6
116.Madsen SK, Gutman BA, Joshi SH, Toga AW,
Jack CR, Jr., Weiner MW, Thompson PM.
Mapping ventricular expansion onto cortical
gray matter in older adults. Neurobiol Aging.
2014 Aug 30
121.Boyle CP, Raji CA, Erickson KI, Lopez OL, Becker
JT, Gach HM, Longstreth WT, Jr., Teverovskiy
L, Kuller LH, Carmichael OT, Thompson PM.
Physical activity, body mass index, and brain
atrophy in alzheimer’s disease. Neurobiol Aging.
2014 Aug 27
122.Prasad G, Joshi SH, Jahanshad N, Villalon-Reina
J, Aganj I, Lenglet C, Sapiro G, McMahon KL,
de Zubicaray GI, Martin NG, Wright MJ, Toga
AW, Thompson PM. Automatic clustering and
population analysis of white matter tracts using
maximum density paths. Neuroimage. 2014 Aug
15;97:284-95
123.Wang B, Petrossians A, Weiland JD. Reduction
of edge effect on disk electrodes by optimized
current waveform. IEEE Trans Biomed Eng. 2014
Aug;61(8):2254-63
124.Shi J, Lepore N, Gutman BA, Thompson PM,
Baxter LC, Caselli RJ, Wang Y. Genetic influence
of apolipoprotein e4 genotype on hippocampal
morphometry: An n = 725 surface-based
alzheimer’s disease neuroimaging initiative
study. Hum Brain Mapp. 2014 Aug;35(8):3903-18
125.Liu W, Rootman DB, Berry JL, Hwang
CJ, Goldberg RA. Methicillin-resistant
staphylococcus aureus dacryoadenitis. JAMA
Ophthalmol. 2014 Aug;132(8):993-5
126.Hong BK, Khanamiri HN, Bababeygy SR, Rao
NA. The utility of routine tuberculosis screening
in county hospital patients with uveitis. Br J
Ophthalmol. 2014 Aug;98(8):1091-5
127.Berry JL, Jubran R, Wong K, Lee TC, Murphree
AL, Kim JW. Factors predictive of long-term
visual outcomes of group d eyes treated with
chemoreduction and low-dose imrt salvage: The
children’s hospital los angeles experience. Br J
Ophthalmol. 2014 Aug;98(8):1061-5
128.Sivakumar RR, Rao NA. Anterior segment
ischemia in viper bite. Ocul Immunol Inflamm.
2014 Apr 30
117.Nir TM, Villalon-Reina JE, Prasad G, Jahanshad
N, Joshi SH, Toga AW, Bernstein MA, Jack
CR, Jr., Weiner MW, Thompson PM. Diffusion
weighted imaging-based maximum density
path analysis and classification of alzheimer’s
disease. Neurobiol Aging. 2014 Aug 27
129.Zito G, Luders E, Tomasevic L, Lupoi D, Toga AW,
Thompson PM, Rossini PM, Filippi MM, Tecchio
F. Inter-hemispheric functional connectivity
changes with corpus callosum morphology
in multiple sclerosis. Neuroscience. 2014 Apr
25;266:47-55
118.Jahanshad N, Nir TM, Toga AW, Jack CR, Jr.,
Bernstein MA, Weiner MW, Thompson PM.
Seemingly unrelated regression empowers
detection of network failure in dementia.
Neurobiol Aging. 2014 Aug 27
130.Chavarria MC, Sanchez FJ, Chou YY, Thompson
PM, Luders E. Puberty in the corpus callosum.
Neuroscience. 2014 Apr 18;265:1-8
119.Hibar DP, Stein JL, Jahanshad N, Kohannim O,
Hua X, Toga AW, McMahon KL, de Zubicaray GI,
Martin NG, Wright MJ, Weiner MW, Thompson
PM. Genome-wide interaction analysis reveals
replicated epistatic effects on brain structure.
Neurobiol Aging. 2014 Aug 27
120.Gutman BA, Wang Y, Yanovsky I, Hua X, Toga
AW, Jack CR, Jr., Weiner MW, Thompson PM.
Empowering imaging biomarkers of alzheimer’s
disease. Neurobiol Aging. 2014 Aug 27
131.Fink C, Borchert M, Simon CZ, Saper C.
Hypothalamic dysfunction without hamartomas
causing gelastic seizures in optic nerve
hypoplasia. J Child Neurol. 2014 Apr 2
132.Wong BJ, Hong BK, Rao NA. Rapid progression
of uveitis and alopecia syphilitica in aids. JAMA
Ophthalmol. 2014 Apr 1;132(4):506-8
133.McHardy SF, Bohmann JA, Corbett MR, Campos
B, Tidwell MW, Thompson PM, Bemben CJ,
Menchaca TA, Reeves TE, Cantrell WR, Jr.,
Bauta WE, Lopez A, Maxwell DM, Brecht KM,
Sweeney RE, McDonough J. Design, synthesis,
and characterization of novel, nonquaternary
reactivators of gf-inhibited human
acetylcholinesterase. Bioorg Med Chem Lett.
2014 Apr 1;24(7):1711-4
134.Braskie MN, Thompson PM. A focus on
structural brain imaging in the alzheimer’s
disease neuroimaging initiative. Biol Psychiatry.
2014 Apr 1;75(7):527-33
135.Storey P, Murchison AP, Dai Y, Hark L,
Pizzi LT, Leiby BE, Haller JA. Comparing
methodologies for imputing ethnicity in an urban
ophthalmology clinic. Ophthalmic Epidemiol.
2014 Apr;21(2):106-10
136.Roussotte FF, Jahanshad N, Hibar DP, Sowell
ER, Kohannim O, Barysheva M, Hansell NK,
McMahon KL, de Zubicaray GI, Montgomery
GW, Martin NG, Wright MJ, Toga AW, Jack CR,
Jr., Weiner MW, Thompson PM. A commonly
carried genetic variant in the delta opioid
receptor gene, oprd1, is associated with smaller
regional brain volumes: Replication in elderly
and young populations. Hum Brain Mapp. 2014
Apr;35(4):1226-36
137.Moysidis SN, Vajzovic L, Gregori G, Goldberg JL.
Acute retinal pigment epithelium detachments
after photocoagulation. Retina. 2014
Apr;34(4):749-60
138.Looi JC, Walterfang M, Nilsson C, Power BD, van
Westen D, Velakoulis D, Wahlund LO, Thompson
PM. The subcortical connectome: Hubs, spokes
and the space between - a vision for further
research in neurodegenerative disease. Aust N Z
J Psychiatry. 2014 Apr;48(4):306-9
139.Li M, Luo XJ, Rietschel M, Lewis CM, Mattheisen
M, Muller-Myhsok B, Jamain S, Leboyer M,
Landen M, Thompson PM, Cichon S, Nothen
MM, Schulze TG, Sullivan PF, Bergen SE, Donohoe
G, Morris DW, Hargreaves A, Gill M, Corvin A,
Hultman C, Toga AW, Shi L, Lin Q, Shi H, Gan
L, Meyer-Lindenberg A, Czamara D, Henry C,
Etain B, Bis JC, Ikram MA, Fornage M, Debette
S, Launer LJ, Seshadri S, Erk S, Walter H,
Heinz A, Bellivier F, Stein JL, Medland SE, Arias
Vasquez A, Hibar DP, Franke B, Martin NG,
Wright MJ, Su B. Allelic differences between
europeans and chinese for creb1 snps and their
implications in gene expression regulation,
hippocampal structure and function, and bipolar
disorder susceptibility. Mol Psychiatry. 2014
Apr;19(4):452-61
140.Fears SC, Service SK, Kremeyer B, Araya C, Araya
X, Bejarano J, Ramirez M, Castrillon G, GomezFranco J, Lopez MC, Montoya G, Montoya P,
Aldana I, Teshiba TM, Abaryan Z, Al-Sharif NB,
Ericson M, Jalbrzikowski M, Luykx JJ, Navarro L,
Tishler TA, Altshuler L, Bartzokis G, Escobar J,
Glahn DC, Ospina-Duque J, Risch N, Ruiz-Linares
A, Thompson PM, Cantor RM, Lopez-Jaramillo C,
Macaya G, Molina J, Reus VI, Sabatti C, Freimer
NB, Bearden CE. Multisystem component
phenotypes of bipolar disorder for genetic
investigations of extended pedigrees. JAMA
Psychiatry. 2014 Apr;71(4):375-87
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141.Dennis EL, Jahanshad N, McMahon KL, de
Zubicaray GI, Martin NG, Hickie IB, Toga AW,
Wright MJ, Thompson PM. Development of insula
connectivity between ages 12 and 30 revealed by
high angular resolution diffusion imaging. Hum
Brain Mapp. 2014 Apr;35(4):1790-800
142.Wong SC, Lee TC, Heier JS. 23-gauge endoscopic
vitrectomy. Dev Ophthalmol. 2014;54:108-19
143.Wong BJ, Hong BK, Samrao D, Kim GH, Rao NA.
A 49-year-old man with unilateral, nontender
left eyelid swelling. Digit J Ophthalmol.
2014;20(1):15-9
144.Walterfang M, Luders E, Looi JC, Rajagopalan
P, Velakoulis D, Thompson PM, Lindberg O,
Ostberg P, Nordin LE, Svensson L, Wahlund
LO. Shape analysis of the corpus callosum in
alzheimer’s disease and frontotemporal lobar
degeneration subtypes. J Alzheimers Dis.
2014;40(4):897-906
145.Stefanini FR, Maia M, Falabella P, Pfister M,
Niemeyer M, Kashani AH, Humayun MS, Koss
MJ. Profile of ocriplasmin and its potential in
the treatment of vitreomacular adhesion. Clin
Ophthalmol. 2014;8:847-56
146.Shi Y, Li J, Toga AW. Persistent reeb graph
matching for fast brain search. Mach Learn Med
Imaging. 2014;8679:306-13
48
of vogt-koyanagi-harada disease: In vivo
documentation. J Ophthalmic Inflamm Infect.
2014;4:9
associated with social cognition and psychotic
symptoms in 22q11.2 microdeletion syndrome.
Front Behav Neurosci. 2014;8:393
151.Meintjes EM, Narr KL, der Kouwe AJ, Molteno
CD, Pirnia T, Gutman B, Woods RP, Thompson
PM, Jacobson JL, Jacobson SW. A tensor-based
morphometry analysis of regional differences
in brain volume in relation to prenatal alcohol
exposure. Neuroimage Clin. 2014;5:152-60
160.Gracanin A, Timmermans-Sprang EP, van Wolferen
ME, Rao NA, Grizelj J, Vince S, Hellmen E, Mol
JA. Ligand-independent canonical wnt activity
in canine mammary tumor cell lines associated
with aberrant lef1 expression. PLoS One.
2014;9(6):e98698
152.Lu PH, Lee GJ, Shapira J, Jimenez E, Mather
MJ, Thompson PM, Bartzokis G, Mendez MF.
Regional differences in white matter breakdown
between frontotemporal dementia and earlyonset alzheimer’s disease. J Alzheimers Dis.
2014;39(2):261-9
161.Fulham WR, Michie PT, Ward PB, Rasser PE,
Todd J, Johnston PJ, Thompson PM, Schall U.
Mismatch negativity in recent-onset and chronic
schizophrenia: A current source density analysis.
PLoS One. 2014;9(6):e100221
153.Lu B, Tai YC, Humayun MS. Microdevicebased cell therapy for age-related macular
degeneration. Dev Ophthalmol. 2014;53:155-66
154.Li J, Shi Y, Toga AW. Diffusion of fiber orientation
distribution functions with a rotation-induced
riemannian metric. Med Image Comput Comput
Assist Interv. 2014;17(Pt 3):249-56
155.Li J, Shi Y, Toga AW. Rotational gradient field for
interpolation of fiber orientation distribution in
connectivity analysis. Proc IEEE Int Symp Biomed
Imaging. 2014;2014:1051-4
147.Schneider C, Helmstaedter C, Luders E,
Thompson PM, Toga AW, Elger C, Weber B.
Relation of callosal structure to cognitive
abilities in temporal lobe epilepsy. Front Neurol.
2014;5:16
156.Lee GJ, Lu PH, Mather MJ, Shapira J, Jimenez
E, Leow AD, Thompson PM, Mendez MF.
Neuroanatomical correlates of emotional
blunting in behavioral variant frontotemporal
dementia and early-onset alzheimer’s disease. J
Alzheimers Dis. 2014;41(3):793-800
148.Sacchet MD, Prasad G, Foland-Ross LC, Joshi
SH, Hamilton JP, Thompson PM, Gotlib IH.
Structural abnormality of the corticospinal tract
in major depressive disorder. Biol Mood Anxiety
Disord. 2014;4:8
157.Kumar R, Farahvar S, Ogren JA, Macey PM,
Thompson PM, Woo MA, Yan-Go FL, Harper
RM. Brain putamen volume changes in newlydiagnosed patients with obstructive sleep
apnea. Neuroimage Clin. 2014;4:383-91
149.Pfister M, Lue JC, Stefanini FR, Falabella P, Dustin
L, Koss MJ, Humayun MS. Comparison of
reaction response time between hand and foot
controlled devices in simulated microsurgical
testing. Biomed Res Int. 2014;2014:769296
158.Jiang X, Tseng CC, Bernstein L, Wu AH. Family
history of cancer and gastroesophageal
disorders and risk of esophageal and gastric
adenocarcinomas: A case-control study. BMC
Cancer. 2014;14:60
150.Nazari H, Hariri A, Hu Z, Ouyang Y, Sadda
S, Rao NA. Choroidal atrophy and loss
of choriocapillaris in convalescent stage
159.Jalbrzikowski M, Villalon-Reina JE, Karlsgodt
KH, Senturk D, Chow C, Thompson PM, Bearden
CE. Altered white matter microstructure is
Photography
Van Urfalian
Printing
Color Graphics
162.Dinov ID, Petrosyan P, Liu Z, Eggert P, Hobel S,
Vespa P, Woo Moon S, Van Horn JD, Franco J,
Toga AW. High-throughput neuroimaging-genetics
computational infrastructure. Front Neuroinform.
2014;8:41
163.Bailey H, Brookes KL, Thompson PM. Assessing
environmental impacts of offshore wind farms:
Lessons learned and recommendations for the
future. Aquat Biosyst. 2014;10:8
164.Ashbrook DG, Williams RW, Lu L, Stein JL, Hibar
DP, Nichols TE, Medland SE, Thompson PM, Hager
R. Joint genetic analysis of hippocampal size in
mouse and human identifies a novel gene linked
to neurodegenerative disease. BMC Genomics.
2014;15:850
165.Apostolova LG, Hwang KS, Kohannim O, Avila
D, Elashoff D, Jack CR, Jr., Shaw L, Trojanowski
JQ, Weiner MW, Thompson PM. Apoe4 effects
on automated diagnostic classifiers for mild
cognitive impairment and alzheimer’s disease.
Neuroimage Clin. 2014;4:461-72
Photo/Image Credits
Cover image courtesy of the Laboratory of Neuro Imaging and Martinos
Center for Biomedical Imaging, Consortium of the Human Connectome
Project-www.humanconnectomeproject.org. Page 2-3 based on image
from the lab of Eun Jin Lee, PhD, USC BME Center for Vision Science and
Technology. Pages 4 upper left and 30 ©John Livzey. Nate Kaiser for Chan
family photos on pages 4 and 14. Pages 9 lower right and 31 from the lab of
Amir Kashani, MD. Page 10 left Abbott Medical Optics, right AqueSys, Inc.
Pages 11 and 21 from the lab of David Hinton, MD. Page 16 from the lab of
Jeannie Chen, PhD. Pages 17 and 27 Replenish, Inc. Page 21 right from the
lab of Mark Humayun, MD, PhD. Page 23 Hardeep Singh, PhD, lab of David
Cobrinik, MD, PhD. Page 29 BostonSight©. Page 32 Springer eBook, David G.
Hunter. Page 35 left Second Sight. Page 36 based on image from the lab of
J. Martin Heur, MD, PhD.
49