indian journal of tuberculosis xxx (xxxx) xxx

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Original article

Study of ocular manifestations in tuberculosis and

its association with HIV AIDS in a tertiary care
hospital

Divya Bisht*, Ranjana Pande

Department of Ophthalmology, BJ Government Medical College, Pune, Maharashtra, India

article info abstract

Article history: Objective: To assess and understand the prevalence and clinical presentation of ocular
Received 13 August 2019 morbidity in patients suffering from tuberculosis and compare it with ocular involvement
Accepted 11 October 2019 in patients coinfected with tuberculosis and HIV AIDS.
Available online xxx Materials and methods: This was a non-comparative, observational, cross sectional study
done on 580 patients, who were diagnosed cases of tuberculosis, pulmonary or extrap-
Keywords: ulmonary, on or off treatment, visiting the Ophthalmology OPD, Tuberculosis OPD and ART
Tuberculosis Centre of the institute in the period from March 2015 to March 2018, screened for ocular
HIV AIDS morbidity.
Ocular manifestations Results: Out of 580, 408 patients had only tuberculosis and 172 had tuberculosis with HIV
AIDS. 108 patients were found to have ocular involvement (18.6%) out of which 63 were
males and 45 were females. The prevalence of ocular morbidity in patients with only
tuberculosis was found to be 16.4% and in those having both tuberculosis and HIV AIDS
was found to be 23.8%.
Conclusion: Our study concludes that posterior uveitis, pan uveitis, periphlebitis and vitritis
are the most common ocular manifestations in tuberculosis. In patients with both tuber-
culosis and HIV most common ocular findings included vitritis and herpes zoster oph-
thalmicus. Our study also concludes that lower CD4 counts (less than 200) in HIV AIDS
patient is significantly associated with ocular involvement.
© 2019 Tuberculosis Association of India. Published by Elsevier B.V. All rights reserved.

Mycobacterium tuberculosis.2 M. tuberculosis is known to invade

1. Introduction
Tuberculosis affects nearly one third of the entire world's
population that is close to 2 million people, out of which only
10% manifest it clinically.1 Tuberculosis is caused by airborne
infection and transmission of an acid fast bacterium known as
and affect any organ of the body, most commonly the lungs.
Ocular involvement by M. tuberculosis usually results due to
haematogenous spread from the lungs.3 M. tuberculosis is an
obligate aerobe and hence tends to grow preferentially in
places where the oxygen tension is high like the choroid and
ciliary body in the eye.4,5

* Corresponding author.
E-mail address: bishtdivya312@gmail.com (D. Bisht).
https://doi.org/10.1016/j.ijtb.2019.10.004
0019-5707/© 2019 Tuberculosis Association of India. Published by Elsevier B.V. All rights reserved.

Please cite this article as: Bisht D, Pande R, Study of ocular manifestations in tuberculosis and its association with HIV AIDS in a tertiary
care hospital, Indian Journal of Tuberculosis, https://doi.org/10.1016/j.ijtb.2019.10.004
2 indian journal of tuberculosis xxx (xxxx) xxx
The association between systemic TB disease and ocular
dissemination has been widely reported, though the incidence
of ocular involvement varies in different studies. Systemic
dissemination has also been reported to significantly increase
the likelihood of ocular lesions up to 60%.6 Though the most
common site of tuberculosis involvement is lungs, the
absence of pulmonary tuberculosis does not rule out the
possibility of ocular tuberculosis.7
Tuberculosis may affect any part of the eye or the adnexal
structures, right from eyelids, conjunctiva, sclera, uvea to
retina, choroid or optic nerve. Eyelid involvement by tuber-
culosis bacilli results in lupus vulgaris, lid abscess or chronic
blepharitis.
Tuberculous conjunctivitis is a chronic disease that usually
affects children and may eventually lead to scarring of the
involved tissue. It also causes phlyctenular keratoconjuncti-
vitis which is a type IV hypersensitivity response to tubercu-
lous protein. Scleral involvement by tuberculosis bacterium
occurs in the form of focal necrotizing scleritis. The most
common anterior segment presentation of tuberculosis
infection is acute or chronic granulomatous anterior uveitis
with mutton fat keratic precipitates occasionally associated
with hypopyon or posterior synechiae. It may cause inter-
mediate uveitis in the form of pars planitis which is evidenced
by vitritis, snowballs, snow banking, peripheral granulomas
and vascular sheathing, often complicated with cystoid
macular edema. The most frequently witnessed posterior
segment involvement by M. tuberculosis occurs in the form of
choroiditis, which may be focal or diffuse. Choroidal
involvement by tuberculosis may also present as subretinal
abscess, choroidal tubercles or tuberculoma. Retinal involve-
ment is usually secondary to choroidal involvement by
tuberculosis bacilli. Primary retinal involvement presents as
vasculitis or Eale's disease. Optic neuropathy can occur due to
infection or inflammation of any part of the optic nerve
throughout its length resulting in disc edema, optic neuritis or
retrobulbar neuritis. If the inflammation is extensive and in-
volves these posterior structures, an endogenous endoph-
thalmitis results when the infection and inflammation
extends through the choroid and retina to involve the
vitreous.
Tuberculosis is an HIV AIDS related opportunistic infection
with atypical clinical features and poor survival. The inci-
dence of tuberculosis has increased with the incidence of HIV
AIDS. The immunocompromised status is responsible for
intense and extensive inflammation and damage to the ocular
structures and also retard recovery in such patients. Drug
malabsorption is another problem with patients suffering
from tuberculosis and HIV AIDS who therefore require pro-
longed drug treatment. The risk of ocular tuberculosis in-
creases rapidly with the fall in CD4 count. Ocular involvement
by tuberculosis bacterium in such patients occurs most
commonly in the form of choroiditis, vitritis and
chorioretinitis.
In order to assess and understand the prevalence and
clinical presentation of ocular morbidity in patients suffering
from tuberculosis and compare it with ocular involvement in
patients co-infected with tuberculosis and HIV AIDS, we
conducted a study in a tertiary care centre.
Please cite this article as: Bisht D, Pande R, Study of ocular manifestations in tuberculosis and its association with HIV AIDS in a tertiary
care hospital, Indian Journal of Tuberculosis, https://doi.org/10.1016/j.ijtb.2019.10.004
2. Materials and methods
The study was approved by the ethical committee of the ter-
tiary care hospital. Patients involved in the study were coun-
selled about it and informed consent was obtained. This was a
non-comparative, observational, cross sectional, single insti-
tution study done on 580 patients, who were diagnosed cases
of tuberculosis, pulmonary or extrapulmonary, on or off
treatment, visiting the Ophthalmology OPD, Tuberculosis OPD
and ART Centre of the institute in the period from March 2015
to March 2018, screened for ocular morbidity. The sample size
was calculated using the formula for prevalence studies, using
95% confidence limit. There is no conflict of interest. Patients
underwent a detailed clinical evaluation of systemic and
ocular complaints. Systemic evaluation was conducted as per
the protocol of Tuberculosis OPD ad ART centre. CD4 counts
were documented in all the patients co-infected with HIV
AIDS and tuberculosis.
Full ophthalmological evaluation was done including,
clinical history, visual acuity screening, colour vision assess-
ment, intraocular pressure estimation, retinoscopy, slit lamp
examination, dilated fundus examination, B scan and OCT,
wherever deemed necessary.
3. Observation and results
The clinical data of 580 patients was evaluated. Out of 580, 408
patients had only tuberculosis and 172 had tuberculosis with
HIV AIDS. 108 patients were found to have ocular involvement
(18.6%) out of which 63 were males and 45 were females. The
prevalence of ocular morbidity in patients with only tuber-
culosis was found to be 16.4% and in those having both
tuberculosis and HIV AIDS was found to be 23.8% (Table 1).
Most common anterior segment ocular involvement was
found to be anterior and intermediate uveitis, whereas vitritis,
multifocal choroiditis and panuveitis were the most
commonly found posterior segment presentations. Peri-
vasculitis and CMV retinitis were the most common posterior
segment pathology found in patients co-infected with tuber-
culosis and HIV AIDS.
4. Discussion
Tuberculosis can affect practically any structure of the eye
and adnexae.8 Ocular manifestations in TB may be attributed
Table 1 e Comparative prevalence of ocular involvement
in patients with tuberculosis and patients co-infected
with tuberculosis and HIV AIDS.
Total Positive ocular Prevalence
patients findings
Only TB 408 67 16.4%
TB with HIV 172 41 23.8%
AIDS
Total 580 108 18.6%
 indian journal of tuberculosis xxx (xxxx) xxx 3

to either infection or non-infectious immunologic reactions.

Table 2 e Distribution of various ocular findings in
Haematogenous dissemination may result in involvement of
patients with TB and in patients co-infected with TB and
the uvea because of its greater vascularity while immuno- HIV AIDS.
logical reactions to tuberculoprotein may cause phlyctenu-
Category Patients with Patients with
losis, interstitial keratitis and retinal vasculitis.5
tuberculosis tuberculosis and
Our study describes the clinical presentation and preva- HIV AIDS
lence of ocular diseases found in patients with tuberculosis
Anterior segment 35.8% (24 patients) 34.1% (14 patients)
and in patients co-infected with tuberculosis and HIV AIDS. Posterior segment 46.2% (31 patients) 58.5% (24 patients)
Out of total 580 patients examined, 408 patients had only Neuro ophthalmic 17.9% (12 patients) 7.3% (3 patients)
tuberculosis and 172 had tuberculosis with HIV AIDS. In total Total 67 patients 41 patients
108 patients were found to have ocular involvement (18.6%)
out of which 63 were males and 45 were females. The preva-
lence of ocular morbidity in patients with only tuberculosis in anterior segment finding in our study. We found seven cases
our study was 16.4% and in those having both tuberculosis of anterior uveitis (10.4%) in patients with tuberculosis, 5 pa-
and HIV AIDS it was found to be 23.8% (Table 1). tients presented with iridocyclitis associated with classic,
According to a study in Spain by Bouza et al,9 the preva- granulomatous, mutton fat keratic precipitates. 2 patients had
lence of ocular involvement in patients with tuberculosis was posterior synechiae with hypopyon (Table 3, Figs. 1 and 2).
found to be 18%. Biswas and Badrinath reported 1.39% inci- Three patients co-infected with HIV AIDS and Tuberculosis
dence of ocular tuberculosis in their study in 1995.10 Mehta showed anterior uveitis with hypopyon (Fig. 1). All these pa-
reported 23.5% incidence of ocular tuberculosis in their study tients had unilateral eye involvement. Gupta et al in their
in 2004.6 study in 2007 found anterior uveitis in 36% of patients with
Babu et al reported 1.95% incidence of concurrent ocular ocular tuberculosis.1 Al-Mezaine et al found anterior uveitis in
tuberculosis in patient with HIV AIDS in India,11 while the 17.9% of patients with ocular tuberculosis.20 Samson and
reported incidence from US was 5%.12 According to Mehta, Foster21 and Gupta et al22 also found anterior granulomatous
systemic dissemination significantly increases the likelihood uveitis with posterior synechiae to be the most common
of ocular lesions up to 60%.6 Extrapulmonary tuberculosis can anterior segment manifestation in tuberculosis in their
be seen in as many as 70% of patients with concomitant studies. A study conducted in a referral centre in north India,
tuberculosis and HIV AIDS.13 by Singh et al, between 1996 and 2001 found 10% of cases
Ocular involvement in tuberculosis was found to show no presenting with uveitis to be secondary to tuberculosis.5
specific age or sex predilection according to our study. It Another study conducted in India in 2013 by Parchand et al
uniformly affected patients of all ages, males and females on uveitis cases found that 9.8% of total uveitis cases were
were equally affected. The majority of cases were chronic. secondary to tuberculosis.23 In India, in a study conducted
These findings are in correspondence with a study done by from January 1992 to December 1994, 0.6% of uveitis cases
Helm and Holland,14 Egbagbe et al,15 Gupta et al,1 and Al- were believed to be caused by tuberculosis.10 In Japan, a pro-
Shakarchi,16 who also found no age or sex predilection in their spective case series from April 1998 to August 2000 reported
studies. that 20.6% of 126 patients with uveitis had a positive purified
Almost three fourth of the patients with ocular involve- protein derivative (PPD) skin test result, and 7.9% were
ment (44 patients), were diagnosed cases of tuberculosis on thought to have intraocular tuberculosis.24 In Saudi Arabia,
systemic anti tuberculous therapy. Patients co-infected with during the period from 1995 to 2000, tuberculosis was the
tuberculosis and HIV AIDS who showed positive findings on cause in 10.5% of uveitis cases seen in a referral centre.25
ocular examination (48 patients) were all on Anti retroviral
therapy, 28 of them were on anti tuberculous treatment. Ma-
jority of the patients had good visual acuity in the better eye at
presentation. Most of these patients showed unilateral Table 3 e Comparison of anterior segment involvement
involvement, supported by study of Al-Shakarchi.16 in patients with tuberculosis and patients co-infected
Both anterior and posterior segment findings were wit- with tuberculosis and HIV AIDS.
nessed, posterior segment involvement being more prevalent Category Patients with Patients with
than anterior segment in both the categories (only tubercu- tuberculosis tuberculosis
losis and tuberculosis with HIV AIDS) (Table 2). This is in and HIV AIDS
accordance with the studies of Gupta et al,1 Al-Shakarchi,16 Anterior uveitis 07 patients (10.4%) 03 patients (7.3%)
Sahu et al,17 Varma et al18 who also found posterior segment Episcleritis/scleritis 01 patient (1.5%) e
involvement to be more common than anterior segment Keratitis 03 patients (4.5%) 05 patients (12.2%- HZO)
Phlyctenulosis 03 patients (4.5%) e
involvement in tuberculosis in their respective studies. A
Allergic 03 patients (4.5%) 03 patients (7.3%)
study in Brazil conducted by Almeida et al19 found anterior
conjunctivitis
segment involvement to be more common than posterior Intermediate uveitis 05 patients (7.5%) e
segment involvement. Dry eye 02 patients (2.9%) 02 patients (4.9%)
Tuberculosis is a well documented cause of anterior uveitis Ocular surface e 01 patient (2.4%)
with mutton fat keratic precipitates, posterior synechiae and squamous
occasional hypopyon. It may also be associated with iris and neoplasia
Total 24 patients 14 patients
angle granulomas.5,10 Anterior uveitis was the most common

Please cite this article as: Bisht D, Pande R, Study of ocular manifestations in tuberculosis and its association with HIV AIDS in a tertiary
care hospital, Indian Journal of Tuberculosis, https://doi.org/10.1016/j.ijtb.2019.10.004
4 indian journal of tuberculosis xxx (xxxx) xxx
Fig. 1 e Anterior uveitis with hypopyon in a patient with
tuberculosis and HIV AIDS.
In Boston, 0.6% of patients with uveitis from 1982 to 1992
were believed to have tuberculosis as an underlying cause.26
Tuberculous pars planitis or intermediate uveitis presents
with vitritis, vitreous snowballs and snowbanking, peripheral
granuloma, vascular sheathing, occasionally complicated
with macular edema. Our study found intermediate uveitis in
5 patients (7.5%) (Table 3). A study of 158 clinic patients with
intraocular tuberculosis in India over a 10-year period by
Gupta et al, found 11 percent of patients with ocular tuber-
culosis to have intermediate uveitis1 Al-Shakarchi in 2015
found 3.2% prevalence of intermediate uveitis in patients with
ocular tuberculosis.16
In a large clinical series of intermediate uveitis from North
India by Parchand et al, tuberculosis was the most common
underlying aetiology seen in 57 (46.7%) of 122 patients with
intermediate uveitis. Presenting signs were vitritis (95 eyes),
snowballs (82 eyes), snowbanking (16 eyes), vascular
sheathing (14 eyes) and healed choroiditis (10 eyes).27
In our study anterior segment manifestations found in
patients co-infected with tuberculosis and HIV AIDS included
Herpes zoster keratitis and ocular surface squamous
neoplasia. 5 patients co-infected with tuberculosis and HIV
AIDS (12.2%) showed herpes zoster keratitis (Table 3, Fig. 3).
Most commonly ocular tuberculosis presents as posterior
uveitis which most often indicates choroidal involvement.
Fig. 2 e Posterior synechiae in a patient with tuberculous
and HIV AIDS.
Please cite this article as: Bisht D, Pande R, Study of ocular manifestations in tuberculosis and its association with HIV AIDS in a tertiary
care hospital, Indian Journal of Tuberculosis, https://doi.org/10.1016/j.ijtb.2019.10.004
We found 9% posterior uveitis, 12% panuveitis and 23.9%
vitritis in patients with tuberculosis in our study (Table 4).
Gupta et al in 2007 found 42% posterior uveitis and 11% pan
uveitis in their study.1 According to study conducted by Al-
Mezaine prevalence of posterior uveitis was found to be 20.5%,
that of pan uveitis was 79.5% and vitritis was 71.2% in patients
with ocular tuberculosis.20
Al-Shakarchi in his study in 2015 found 92.1% pan uveitis,
4.7% posterior uveitis and vitritis universally in all the patients
with tubercular uveitis.16
The presence of choroidal lesions, with or without
inflammation, is strongly correlated with systemic disease,
and is an indicator of haematogenous spread of mycobac-
teria.28 Choroidal involvement due to M. tuberculosis may be in
the form of choroiditis, subretinal abscess, tubercles or
tuberculomas.
Multifocal choroiditis was found to be the most common
presentation of posterior segment involvement in our study
which is supported by study of Bastion in 2004 and Tabbara in
2007.2 Al-Shakarchi also found multifocal choroiditis to be the
most common mode of presentation in patients with TB
uveitis (82.5%) in his study in 2015.16 Multifocal choroiditis
was found in 7 patients (6 unilateral and 1 bilateral e 10.4%)
with only tuberculosis and 3 patients (7.3%) with tuberculosis
and HIV AIDS. Al-Mezaine found 20.5% prevalence of multi-
focal choroiditis in patients with ocular tuberculosis in his
study in 2008.20
We found choroidal tubercles in 2 patients (3%) with
tuberculosis (Table 4). Choroidal tubercles were generally less
than half disc diameter in size, multiple, involving mostly the
posterior pole, yellowish in colour without distinct boundaries
(Fig. 4).
In Malawi, Africa, a 2.8% incidence of choroidal tubercles in
109 patients with fever and tuberculosis was reported in a
prospective study in 2002.29
Primary involvement of retina occurs in the form of
vasculitis or Eale's disease.
We found periphlebitis in 4 patients (6%) with associated
vitritis and retinal haemorrhages and Eale's disease in 2 pa-
tients, both young males (Table 4).
Al-Mezaine found periphlebitis in 35.6% of patients in his
study in 2008.20
Fig. 3 e Herpes zoster ophthalmicus in a patient co-
infected with tuberculosis and HIV AIDS.
 indian journal of tuberculosis xxx (xxxx) xxx 5

Table 4 e Comparison of posterior segment involvement

in patients with tuberculosis and patients co-infected
with tuberculosis and HIV AIDS.
Category Patients with Patients with
tuberculosis tuberculosis
and HIV AIDS
Multifocal choroiditis 07 patients (10.4%) 03 patients (7.3%)
Retinitis e 04 patients (9.8%-
CMV)
Macular edema 01 patient (1.5%) e
Eales disease 02 patients (3%) e
Vitritis 16 patients (23.9%) 04 patients (9.8%)
Posterior uveitis 06 patients (9%) e
Perivasculitis 04 patients (6%) 04 patients (9.8%) Fig. 5 e CMV Retinitis in a patient coinfected with HIV AIDS
Panuveitis 08 patients (12%) e and tuberculosis.
Cotton wool spots e 02 patients (4.9%)
Retinal haemorrhages e 03 patients (7.3%)
Toxoplasma e 01 patient (2.4%)
Acute retinal necrosis e 02 patients (4.9%)
Endophthalmitis 01 patient (1.5%) e In patients with HIV AIDS, choroidal tubercles may be
Choroidal tubercles 02 patients (3%) 01 patient (2.4%) asymptomatic with little overlying vitritis and detected on
Total 31 patients 24 patients
routine examination.30
Babu et al documented choroidal granuloma in 52.63% and
choroidal abscess in 36.84% in his study on patients with
Gupta et al described 13 patients with retinal vasculitis and tuberculosis and HIV AIDS.11
a PCR result positive for tuberculosis in the aqueous or vitre- Tubercular spread into the optic nerve can be secondary to
ous fluid, further strengthening the association between choroidal involvement or due to haematogenous seeding. Any
tuberculosis and retinal vasculitis.1,28 part of the entire length of the nerve can be involved resulting
In my study 4 patients with both tuberculosis and HIV AIDS in disc edema, optic neuritis or retrobulbar
showed classic CMV retinitis (Fig. 5), 1 patient had toxo- neuritis. Tubercular optic neuropathy is usually seen as ret-
plasma, 2 patients showed acute retinal necrosis (Table 4). robulbar optic neuritis complicating tubercular meningitis.
Both M. tuberculosis and atypical mycobacteria cause sys- 3 patients in my study with meningeal tuberculosis
temic and ocular morbidity in immunocompromised in- showed disc edema, 2 had retrobulbar neuritis. We also wit-
dividuals, including massive choroidal infiltrates, choroidal nessed 3 cases of drug induced optic neuritis, all suffering
nodules, vitritis, endophthalmitis, nonreactive choroidal from multidrug resistant tuberculosis (Table 5) We found optic
tuberculoma, choroiditis, multifocal choroiditis (Fig. 6) and atrophy in 1.5% of patients (Table 5). Egbagbe found optic at-
chorioretinitis.30 rophy in 1.1% patients in his study in 2006.15
Tuberculous choroiditis has been reported in patients with HIV infection is a significant risk factor for tuberculosis.
AIDS and systemic tuberculosis. We found choroiditis in 3 There are multiple case reports of HIV patients with biopsy or
patients (7.3%), choroidal tubercles in 1 patient (2.4%), co- culture proven systemic TB who do not respond to tuberculin
infected with tuberculosis and HIV AIDS,in our study (Table 4). skin testing, therefore tuberculin skin testing is not reliable in
this group. Not only does their immunocompromised status

Fig. 4 e Choroidal tubercles in a patient with tuberculosis. Fig. 6 e Choroiditis in a patient with tuberculosis.

Please cite this article as: Bisht D, Pande R, Study of ocular manifestations in tuberculosis and its association with HIV AIDS in a tertiary
care hospital, Indian Journal of Tuberculosis, https://doi.org/10.1016/j.ijtb.2019.10.004
6 indian journal of tuberculosis xxx (xxxx) xxx

Table 5 e Comparison of neuro-ophthalmic involvement Conflicts of interest

in patients with tuberculosis and patients co-infected
with tuberculosis and HIV AIDS.
The authors have none to declare.
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care hospital, Indian Journal of Tuberculosis, https://doi.org/10.1016/j.ijtb.2019.10.004
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Please cite this article as: Bisht D, Pande R, Study of ocular manifestations in tuberculosis and its association with HIV AIDS in a tertiary
care hospital, Indian Journal of Tuberculosis, https://doi.org/10.1016/j.ijtb.2019.10.004