s u r v e y o f o p h t h a l m o l o g y 5 9 ( 2 0 1 4 ) 4 6 8 e4 7 3

Available online at www.sciencedirect.com

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journal homepage: www.elsevier.com/locate/survophthal

Clinical challenges

HIV and cannot see

Claudia M. Prospero Ponce, MDa, Nagham Al Zubidi, MDb,

Hilary A. Beaver, MDb,c, Andrew G. Lee, MDb,d,*, Derrick A. Huey, MDe,
Pamela S. Chavis, MDe
a
Department of Pathology and Genomic Medicine, Ocular Pathology, Houston Methodist Hospital, Houston, TX
b
Department of Ophthalmology, Houston Methodist Hospital, Houston, TX
c
Department of Ophthalmology, Weill Cornell Medical College, Houston, TX
d
Departments of Ophthalmology, Neurology, and Neurosurgery, Weill Cornell Medical College, Houston, TX
e
Department of Ophthalmology, Medical University of South Carolina, Charleston, SC

article info (In keeping with the format of a clinical pathological conference, the abstract and key words appear
at the end of the article.)
Article history:
Received 11 October 2013
Accepted 11 October 2013
Available online 20 May 2014
Peter Savino and Helen Danesh-
Meyer, Editors

1. Case report and docusate sodium. He admitted to cigarette smoking,

A 55-year-old white man presented with acute painless visual
loss in his right eye. An ophthalmologist diagnosed uveitis OD.
Human immunodeficiency virus (HIV) testing was positive. He
was started on highly active antiretroviral therapy (HAART),
but was noncompliant. He was referred for consultation two
weeks later because of altered mental status, continued vision
loss OD, and dysphagia. He denied arthralgias, myalgias,
fever, night sweats, or weight loss. His CD4 count was 174
cells/mm3 and the viral load >10,000,000 copies. His medica-
tions included: emtricitabine, tenofovir, sulfamethoxazole-
trimethoprim double-strength, darunavir, pyrimethamine,
acyclovir, leucovorin, sulfadiazine, albuterol, ipratropium,
zolpidem, hydrocodone/acetaminophen, ibuprofen, ondase-
tron, promethazine, acetaminophen, diphenhydramine, hy-
dralazine, aluminum magnesium hydroxide, simethicone,
alcohol intake (amount unknown), and methamphetamine
use. He had been married for 30 years, but reported multiple
male to male sexual contacts.
He was alert and oriented to person and place, but not to
time, and was only intermittently arousable. Visual acuity was
light perception OD and 20/100 OS. The pupils measured
3.5 mm bilaterally with a right relative afferent pupillary defect
(RAPD). Confrontation visual field testing was normal OS. There
were questionable abduction and adduction defects OD, but the
cooperation of the patient was compromised by his mental
status. Slit-lamp examination showed moderate conjunctival
chemosis with diffuse, moderate- to large-sized, mutton-fat
granulomatous keratitic precipitates OD. No Koeppe or Busacca
iris nodules were seen, and the rest of the anterior segment
was normal OU. Intraocular pressures were 23 mm Hg OD and
19 mm Hg OS. Diffuse cream-colored suspended cells in the

* Corresponding author: Andrew G. Lee, MD, Department of Ophthalmology, Houston Methodist Hospital, 6560 Fannin Street, Scurlock
450, Houston, Texas 77030.
E-mail address: AGLee@tmhs.org (A.G. Lee).
0039-6257/$ e see front matter ª 2014 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.survophthal.2013.10.003

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 s u r v e y o f o p h t h a l m o l o g y 5 9 ( 2 0 1 4 ) 4 6 8 e4 7 3 469

vitreous obscured further visualization of the optic nerve and unusual infections such as Aspergillus and Candida endoph-
retina OD; the fundus was unremarkable OS. thalmitis, but they would have disseminated disease with
What is the differential diagnosis with the information given? positive chest imaging and/or blood cultures.31,34 PCR of the
What further investigation(s) would you perform? aqueous could be considered for Aspergillus, Cryptococcus, or
Candida since vitreous samples are positive in only 38% of
1.1. Comments by Pamela Chavis, MD patients.31,35 HIV-associated autommune disease may
include sarcoidosis so a serum angiotensin converting
Anterior uveitis with vitritis may be caused by a gamut of enzyme (ACE) test is required; only 30e40% have a positive
diseases, spanning infections, malignancies, autoimmune serum test, however, but 50e75% can have a positive CSF
diseases, and even trauma.3 The list of potential infectious ACE.32
causes is also vast, including mycobacteria, Lyme disease, Computed tomography (CT) of the chest can be helpful in
toxocariasis, toxoplasmosis, syphilis, parasitic infections, and diagnosing tuberculosis, sarcoidosis, and fungal disease and
even certain fungal infections.1,12,24,27,28,31,34,36e38 Given such may identify a lesion to biopsy. Ocular mycobacterial disease
a long and varied list, it is useful to group these infections by can be isolated, however, and only approximately 47% may
their anterior chamber presentation. Infections with eye have chest imaging consistent with granulomatous disease.28
involvement may show both granulomatous and non- CT scan of the chest shows hilar adenopathy more frequently
granulomatous anterior uveitis. When considering only the in neurosarcoid and is more sensitive than routine chest ra-
former, the list can be narrowed. Mycobacteria, Lyme disease, diographs.32 CT scans of the pelvis, abdomen, and bone
and syphilis are common infectious entities that present with marrow for lymphoma have a low yield unless the patient has
granulomatous uveitis and must be ruled out.1,28,37 There has systemic signs.8 MRI of brain and orbit, with and without
also been a case report of a presumed parasitic granuloma in contrast, is essential to further evaluate the left eye with the
the anterior chamber angle presenting with granulomatous visual acuity of 20/100, and also to evaluate the altered
uveitis.36 mentation.
The posterior pole in the right eye could not be visualized,
and there was an RAPD as well. Vitritis alone would not pro-
duce an RAPD, so a B-scan ultrasound needs to be done to rule
out retinal detachment, choroidal mass, retinal granuloma, or 2. Case report (continued)
optic nerve head swelling. Retinal detachment can occur with
toxoplasmosis, lymphoma, syphilitic posterior uveitis, or a CT scan of the head showed nonspecific periventricular
mass, (e.g., toxoplasmosis or toxocara can be associated with hypodensities in the white matter of the frontal region.
tractional retinal detachment).18,38 Granuloma could suggest Magnetic resonance imaging (MRI) of the head and orbit
sarcoidosis, mycobacterial, fungal, lymphoma or toxocara showed choroidal thickening OD (Fig. 1) and areas of
(parasitic) involvement. abnormal increased signal involving the anterior caudate
Chorioretinitis with local swelling, retinalechoroidal nuclei, the anterior limbs of the internal capsules, the white
thickening, or retinal detachment on B-scan ultrasound can
occur with lymphoma, syphilis, toxoplasmosis, Lyme disease,
cat scratch disease (CSD), or fungal disease.14 Papillitis can
occur with syphilis, toxoplasmosis, CSD, and Lyme disease.
Uveitis from syphilis in HIV-positive occurs in less than 1% of
these patients, however, and a dense vitritis is atypical.15 A
severe unilateral granulomatous panophthalmitis can be
found in any of the aforementioned etiologies, including
parasitic infection.
The decreased visual acuity OS may be attributable to the
patient’s altered mentation, but a confrontation visual field
could be helpful. The altered mentation raises the question of
systemic infection or central nervous system disease.
At this point, checking for infectious etiologies is neces-
sary. A small study of tuberculosis (TB)-related intraocular
inflammation by Patel et al found 92% of patients with iso-
lated ocular disease tested positive with a tuberculin skin
test, and 86% were positive with the QuantiFERON-TB Gold
In-Tube test.28 Likewise, serologic testing for syphilis exists
in the form of serum VDRL, FTA-ABS, and RPR, but cere-
brospinal fluid (CSF) analysis with VDRL testing may be
more appropriate in HIV patients with posterior uveitis.
Additionally, patients with HIV and syphilis were more
likely to have CSF abnormalities than HIV-negative patients Fig. 1 e Brain MRI, axial section T1 post contrast, showing
with syphilis.1 Lyme disease may be diagnosed by ELISA or choroidal thickening and enhancement relative to the
by PCR of serum or CSF.24 HIV-positive patients may have fellow eye (arrow).

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2022. Para uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2022. Elsevier Inc. Todos los derechos reservados.
470 s u r v e y o f o p h t h a l m o l o g y 5 9 ( 2 0 1 4 ) 4 6 8 e4 7 3
Fig. 2 e Brain MRI, axial section T2, showing
hyperintensity of the caudate nucleus bilaterally (arrows)
and periventricular white matter.
matter lateral to the anterior caudate nuclei bilaterally, the
septum pellucidum, hypothalamus, anterior thalamus on the
right, and a large portion of the thalamus on the left
extending laterally to involve the optic radiations bilaterally
Fig. 3 e Brain MRI, axial section T2, showing bilateral
symmetric thalamic hyperintensity.
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2022. Para uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2022. Elsevier Inc. Todos los derechos reservados.
Fig. 4 e Brain MRI, coronal section T1 post contrast,
showing areas of enhancement along the optic chiasm,
proximal optic tracts and hypothalamic region (arrow).
(Figs. 2 and 3). There was gadolinium enhancement of the
optic chiasm, proximal optic tracts, and hypothalamic region
(Fig. 4), along with the ependymal and subependymal regions
of the frontal horns and, to a lesser extent, around the third
ventricle.
What further evaluation should be done?
2.1. Comments by Dr. Chavis (continued)
HIV patients with central nervous system (CNS) signs and
symptoms are fairly common. In one study, up to 44% of HIV-1
patients were found to have CNS disease with a mortality rate
in these patients of 49% and median survival of 0.2 years.11,16
Cerebrospinal fluid analysis is an important next step for
analysis of potential infection, or autoimmune disease
concomitant with HIV, and it needs to include flow-cytometry
for lymphoma.
Additionally, CNS involvement in systemic AIDS-related
lymphoma is high at 21.7%.39 Toxoplasmosis and CNS lym-
phoma, however, may present similarly on imaging.26 For
this reason, a logical next step may be serologic or CSF
analysis for Epstein-Barr virus (EBV). In addition to plasma,
EBV-DNA, CSF EBV-DNA, or PCR may be useful in identifying
this subset of patients, especially when applied in a quanti-
tative manner, with a specificity of near 100%.26,39 Neuro-
sarcoidosis commonly involves the basilar meninges. A case
report demonstrates the potential for using 18-fluorodeoxy-
 s u r v e y o f o p h t h a l m o l o g y 5 9 ( 2 0 1 4 ) 4 6 8 e4 7 3 471

Fig. 5 e Histological analysis of diffuse large B-cell CNS lymphoma. Hematoxylin and eosin stain: A: Section showing a small
portion of brain tissue with large atypical tumor cells around and infiltrating the vessel (star). B: High magnification of the
tumor showing mitotic figures and polymorphic nucleous (arrow) compared to the normal lymphocyte (dashed arrow).
Immunohistochemical stains: C: CD20 stain positivity (brown), indicating B-cell origin. D: High proliferation factor (Ki67)
stain positivity (dark brown), showing the high proliferation of neoplastic cells.

glucose positron emission to identify lymph nodes for
biopsy.23
3. Case report (continued)
Serum rapid plasma reagin (RPR) and fluorescent treponemal
antibody absorbed test (FTA-ABS) were negative. Toxoplas-
mosis and cryptococcal IgM/IgG titers and Quantiferon TB
Gold were negative. The CSF showed modestly elevated CSF
protein, but was negative for TB, CMV, Cryptococcus or Toxo-
plasma antigens.
What should be done next?
3.1. Comments by Dr. Chavis (continued)
PET scan can be considered because tumors classically man-
ifest increased metabolism, but inflammations such as
sarcoidosis and infections including fungal disease may also
show increased metabolism. Similarly, proton magnetic
resonance spectroscopy may show overlapping patterns for
tumors and tuberculoma, with variable readings for fungal
and other infections.26 If testing for infectious etiologies is
negative, further imaging may not help. Then direct sampling
is essential. If a patient has ophthalmic manifestations, it may
also be possible to diagnose CNS lymphomas by vitreous bi-
opsy. Pars plana vitrectomy is an invaluable tool in the diag-
nosis of panophthalmic disease. By taking a small vitreous
sample or running infusion fluid for cytologic analysis, the
diagnosis of CNS lymphoma may be made, and the patient
spared a brain biopsy.19 Atypical cells may be identified, and
cytokine analysis with a ratio of IL-10/IL-6 greater than 1.0 is
suggestive of intraocular lymphoma.19 EBV in situ hybridiza-
tion of a vitreous sample may also point to a CNS lymphoma
and could potentially save the patient a trip to the operating
room with the availability of bedside vitrectomy.25 Chorior-
etinal biopsies can also be done trans-sclerally or by fine-
needle aspiration of a choroidal mass.29
4. Case report (concluded)
While hospitalized, the patient developed adrenal insuffi-
ciency, diabetes insipidus, and hypothyroidism requiring
medical replacement therapy. One week later, the MRI
showed progression of the multifocal, contrast-enhancing,
periventricular hyperintense deep brain lesions. An endo-
scopic brain biopsy found diffuse large B-cell lymphoma. EBV
testing was negative (Fig. 5). Intrathecal chemotherapy was
initiated with methotrexate and cytarabine, but the patient’s
mental status and medical condition continued to deteriorate.
He received whole brain radiation, but after the fifth cycle, he
developed pancytopenia, neutropenic fever, and septic shock
and expired after being transferred for palliative care.
5. Discussion
Our patient had biopsy-proven diffuse large B-cell lymphoma.
The incidence of primary CNS lymphoma (PCL) in HIV patients
is 2e6%,10 up to 10% in autopsy series,17 and has increased
since the introduction of HAART.20

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472 s u r v e y o f o p h t h a l m o l o g y 5 9 ( 2 0 1 4 ) 4 6 8 e4 7 3
Although PCL represents only 1% of non-Hodgkin lym-
phoma (NHL) in the general population, it is as high as 15% in
HIV-infected patients.9 The UK Collaborative HIV Cohort re-
ported a CD4 count of approximately 200 cells/mm3 in pa-
tients with systemic NHL.7 NHL can produce variable
ophthalmic findings including uveitis,30 ptosis, lid edema,
proptosis, and ophthalmoplegia.21
Although MRI is helpful in the diagnosis of PCL, these le-
sions can mimic intracranial infections in AIDS, especially
toxoplasmosis.13 Therefore, serologic studies and CSF analysis
are needed to rule out toxoplasmosis. Stereotactic brain bi-
opsy may be required for diagnosis.33 In cases where definitive
brain biopsy cannot be performed, measurement of EBV DNA
in CSF and CSF cytology may be an alternative for making the
diagnosis.4,22 EBV DNA in CSF can also be used as a marker of
response to treatment.2 In addition, conventional CSF
cytology and flow cytometry can be diagnostic of PCL.4 The
presence of a soluble B-cell marker CD23 (Scd23) in CSF can
also help in the diagnosis of AIDS-related lymphoma and has
been reported to have a sensitivity of 77% and specificity of
94%.6 The current treatment of AIDS-related PCL is chemo-
therapy with or without radiation therapy, but the disease is
frequently fatal despite aggressive therapy.5
6. Method of literature search
The literature search was performed using Medline (OvidSP,
EBSCO), UpToDate, and PubMed, and the following search
terms: uveitis in HIV, uveitis in AIDS, opportunistic infections in
HIV, HIV lymphoma, drug-induced uveitis, non-Hodgkin lymphoma,
and HIV.
Case reports were only included if they provided relevant
information about characteristics and diagnosis of the dis-
ease. We included all relevant articles published after 1981
when the first HIV case was reported.
7. Disclosure
The authors report no proprietary or commercial interest in
any product mentioned or concept discussed in this article.
Acknowledgments
We would like to recognize Dr. Andreana Rivera for her
contribution with the pathology slides and immunohisto-
chemistry analyses.
This work was supported in part by an unrestricted grant
from Research to Prevent Blindness, Inc., New York, NY.
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Descargado para Álvaro Loza Sierra (alvaroloza1995@gmail.com) en Marques de Valdecilla Foundation de ClinicalKey.es por Elsevier en noviembre 09,
2022. Para uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2022. Elsevier Inc. Todos los derechos reservados.
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abstract

Keywords: A 55-year-old HIV-positive man presented with acute vision loss in the right eye and
HIV altered mental status. Ophthalmic evaluation revealed light perception vision OD with a
HAART right relative afferent pupillary defect, conjunctival chemosis, large mutton-fat keratitic
panophthalmitis precipitates, and diffuse cream-colored vitreous cells. Magnetic resonance imaging of the
uveitis brain and orbit with and without contrast with fat saturation showed choroidal thickening
opportunistic infections OD, multifocal deep periventricular and deep ganglionic enhancing lesions, and a supra-
CNS lymphoma sellar mass. Brain biopsy showed diffuse large B-cell lymphoma. Intrathecal chemotherapy
with methotrexate and cytarabine and whole brain radiation therapy failed. His mental
status deteriorated. He developed pancytopenia, neutropenic fever, and septic shock and
subsequently expired under palliative care.
ª 2014 Elsevier Inc. All rights reserved.

Descargado para Álvaro Loza Sierra (alvaroloza1995@gmail.com) en Marques de Valdecilla Foundation de ClinicalKey.es por Elsevier en noviembre 09,
2022. Para uso personal exclusivamente. No se permiten otros usos sin autorización. Copyright ©2022. Elsevier Inc. Todos los derechos reservados.