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tuberculosis/

Review Article

Ocular manifestations of tuberculosis

J.L. Goyal a,*, Parul Jain b, Ritu Arora a, Pallavi Dokania c

a
Director Professor, Guru Nanak Eye Centre, Maulana Azad Medical College, New Delhi 110002, India
b
Senior Resident, Guru Nanak Eye Centre, Maulana Azad Medical College, New Delhi 110002, India
c
Junior Resident, Guru Nanak Eye Centre, Maulana Azad Medical College, New Delhi 110002, India

article info abstract

Article history: Tuberculosis (TB) is a chronic debilitating infection which is caused by Mycobacteriumn
Received 31 December 2014 tuberculosis and other mycobacteria. Mycobacterium tuberculosis affects predominantly the
Accepted 7 April 2015 lungs although it can affect every organ of the body. Two billion people are affected by
Available online xxx tuberculosis. Majority of tuberculosis cases and related deaths occur in Asia.1 Tuberculosis
most commonly occurs in people belonging to the low socio-economic status. Crowding,
Keywords: poor healthcare, unemployment and poor knowledge about basic sanitation increase the
Ocular tuberculosis risk of acquiring the infection. India is endemic for tuberculosis with 256/lakh population.2
Manifestations TB can affect majority of the structures of the eye with marked variability of the lesions.
Differential diagnosis This review will focus on the clinical presentation and management of ocular TB.
© 2015 Tuberculosis Association of India. Published by Elsevier B.V. All rights reserved.

The term “ocular tuberculosis” is used to describe infections The pathogenesis of ocular TB involves 5 stages and is
caused by Mycobacterium tuberculosis or any of the three summarized below3e5:-
other mycobacteria species (sp. bovis, africanum, and microti)
Droplet nuclei with mycobacteria are inhaled
in the eye. The bacteria affects the eye either by a direct
invasion after haematogenous dissemination accompanied The organism then passes downthrough the bronchial tree and enters the alveolus
by local inflammation, or via a hypersensitivity reaction to
the bacteria with a focus elsewhere in the body. The factors The bacteris is then phagocytosed by alveolar macrophages
that increase the risk of acquiring TB are:
There is monocyte recruitment to the site, leading to

Age (young< 5 yrs and elderly men are at an increased risk). A Delayed type hypersensitivity response – tissue damage- caseous necrosis

Alcoholism and/or drug addiction.

HIV infection.

Diabetes mellitus.
Good cell mediated immunity poor cell mediated immunity

Immunosuppressive conditions.

Close contact with patients harboring active infection. Halt progression liquefaction and caseousnecrosis

Silicosis

Poverty and malnutrition.

* Corresponding author. Guru Nanak eye centre, Maulana Azad Medical College, New Delhi 110003, India. Tel.: þ91 9968604330, þ91 (011)
23235145.
E-mail address: [email protected] (J.L. Goyal).
http://dx.doi.org/10.1016/j.ijtb.2015.04.004
0019-5707/© 2015 Tuberculosis Association of India. Published by Elsevier B.V. All rights reserved.

Please cite this article in press as: Goyal JL, et al., Ocular manifestations of tuberculosis, Indian Journal of Tuberculosis (2015),
http://dx.doi.org/10.1016/j.ijtb.2015.04.004
2 i n d i a n j o u r n a l o f t u b e r c u l o s i s x x x ( 2 0 1 5 ) 1 e8

The respiratory tract is the most common portal of entry for 2.2. Orbital tuberculosis-10e13
infectious droplet nuclei that spread by coughing or sneezing.
The bacteria are ingested by alveolar macrophages and Orbial TB can occur as ahaematogenous spread or contiguous
multiply within these phagocytes eventually destroying them. spread from the neighbouring paranasal sinuses. Manifesta-
The infected macrophages spread by lymphatic flow to the tions of orbital TB can be grouped under five clinical groups:
regional lymph nodes and then enter the haematogenous route.
- Orbital Periostitis,
- Orbital soft tissue tuberculoma without bony destruction,
- Orbital tuberculoma with bony involvement,
1. Clinical spectrum of intraocular TB
- Orbital spread from paranasal sinuses and dacryoadenitis.
a) Orbital periostitis: It affects the people in the first two de-
All parts of the eye maybe affected by TB. The most common
cades of life as maximum bone growth occurs during these
ocular manifestations are chorioretinitis and uveitis.

2. Tuberculosis of the adnexa years. It presents as erythema and edema of the lids and
conjunctiva with involvement of the spongy vascular tis-
2.1. Skin of eyelids and peri-orbital area6e9 sue of the outer margin of the orbit. It is the most common
type of orbital TB and can lead to the formation of a
a) Lupus vulgariseA chronic form of adnexal tuberculosis that chronically discharging fistula.
affects eyelid skin and occurs in patients who are sensitive b) Tuberculomas of the orbit present as a painless proptosis
to tuberculin antigen. The lesions are solitary, small, reddish with or without involvement of bones.
brown usually involving the head and neck region and have c) Orbital abscesses
gelatinous consistency (Apple jelly nodules).
b) Tubercular lidseLesions are popular or indurated nodules
or plaque which may ulcerate. 2.3. Lacrimal system
c) Erythema nodosumeReddish nodules on the lids.
d) ScrofulodermaeLesions are firm, painless nodules that a) Non specific dacryoadenitis with or without abscess for-
overly a tuberculous focus which may break down and mation is a usual presentation in these cases.
suppurate leading to ulcer formation with undermined b) Chronic dacryocystitis can present in two forms
edges and granulation tissue at the floor. Healing of ulcers 1. Attenuated sclerotic form: It presents as chronic
is slow and indolent. painless hard lobulated mass associated with limitation
e) TarsitiseInflammation of the tarsal plate of the lids. of extra-ocular movements and ptosis or proptosis.
f) Miliary TB of the skinePresents as multiple small red 2. Active caseous form presenting as red and edematous
papules or macules in cases with fulminant military TB. lesion of lids with fluctuation and fistulization.

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2.5. Cornea

a) Phlyctenular Keratoconjunctvitis: The patients usually

present with a gritty sensation and photophobia. The
lesions are usually present at the limbus and appear as
small pink colored nodules and they may progress cen-
trally accompanied by a leash of superficial vessels.
These lesions can ulcerate. The condition is
described as a hypersensitivity reaction to the tubercular
proteins (Fig. 2).

b) Intersitial keratitis: The Interstitial keratitis presents as

Fig. 1 e Clinical photograph showing conjunctival chemosis peripheral stromal vascularised infiltrate involving super-
and nodule in a patient with active pulmonary TB. ficial and middle layers of the cornea. Attacks are recur-
rent. It is a hypersensitivity reaction to tubercular proteins
(Fig. 3).

2.4. Conjunctiva14e17
2.6. Sclera and episclera
- Phlyctenulosis is the most common manifestation of
tuberculosis which may involve the conjunctiva alone or Episcleral nodules may form due to a reaction to the myco-
it may involve the cornea along with conjunctiva near the bacterium protein.
limbus. Tuberculomas, ulceration and nodules of Scleral involvement can be diffuse or nodular. Focal
conjunctiva are very rare. The usual presentation is necrotizing anterior scleritis is the most common presenta-
that of an unilateral conjunctivitis with associated lym- tion of tubercular scleritis. Scleral perforation can occur
phadenitits (Fig. 1). because of necrosis (Fig. 4).

Fig. 2 e (A) Cinical photograph of a patient with sterile perforation with peripheral sclerokeratitis secondary to TB. (B)
Superior corneal thinning with phlyctenularkerato conjunctivitis.

Fig. 3 e Clinical photographs depicting interstitial keratitis in patients with TB.

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associated exudative retinal detachment. There may be

haemorrhages on the surface of tuberculoma.
c) Subretinal abscesseThese lesions are usually seen in
patients with disseminated tuberculosis. There is min-
imal vitreous inflammation. They are yellowish in
colour indicating liquefaction necrosis.
d) Serpeginous like choroiditiseIt is a chronic recurrent
inflammation of the choroids and choriocalliparies.
Retina may be involved at later stages. It begins in the
peripapillary region and is presumed to be autoimmune
in nature. It may be due to an immune mediated hy-
persensitivity reaction to the bacteria in the or choroid
Fig. 4 e Nodular scleritis in a patient with miliary
retinal pigment epithelium (Fig. 5).
tuberculosis.
e) Retinal vasculitiseInflammation of the retinal vessels is a
known association of systemic TB, more commonly
involving the veins than arteries. Active vasculitis is seen
as severe perivascular cuffing, infiltrates, retinal hemor-
2.7. Uvea17e22 rhages, moderate vitritis, snowball opacities, neuroretinitis
and focal choroiditis. Presence of perivascular choroiditis
The most common presentation of intraocular tuberculosis in
lesions (active or healed) is a strong indicator of tubercular
the eye is uveitis. The presentation varies from anterior uve-
etiology. TB retinal vasculitis may first present with vitre-
itis to panuveitis.
ous/preretinal hemorrhage. Tubercular retinal vasculitis
and Eales disease are associated with extensive peripheral
a) Anterior uveitis:
capillary closure. The presence of associated active or
healed patches of focal choroidits along the retinal veins
The patients present with a unilateral or bilateral uveitis. It
help differentiating TB from Eales disease, sickle cell and
is a chronic, recurrent granulomatous condition and large,
Behchets disease(Fig. 6).
mutton fat keratic precipitates are usually present. Iris nod-
f) Neuroretinitis and optic neuropathyeThe optic nerve may
ules may be seen. Koeppe's nodules are seen at the papillary
be affected and the manifestations can be in the form of an
border and Bussacas nodules are seen on the iris surface. The
optic nerve tubercle, papillitis, papilloedema, optic
uveitis is complicated by the development of cataract, poste-
neuritis, retrobulbar neuritis and neuroretinitis.
rior synechiae and maybe accompanied by inflammation in
g) Endophthalmitis and panophthalmitiseThis form of dis-
the posterior segment.
ease shows rapid progression with destruction of intraoc-
ular tissue. When choroidal and subretinal abscesses are
b) Intermediate uveitis:
left untreated, they undergo liquefaction necrosis with
rapid multiplication of acid fast bacilli and can eventually
Vitreous inflammation presents with moderate to severe
burst into the vitreous cavity, presenting as endoph-
cellular reaction in the vitreous cavity, including snowball
thalmitis or panophthalmitis.
opacities. The most frequent complications related to TB-
uveitis included cystoid macular edema (40%) and cataract
(38.9%). Other less common complications were epiretinal
membrane, raised intraocular pressure, optic disc pallor, pe-
ripheral neovascularization, retinal detachment and vitreous
hemorrhage.

c) Posterior uveitiseTB can present as posterior uveitis or

hypersensitivity retinal vasculitis in the form of Eales dis-
ease or primary vasculitis per se. The tuberculous posterior
uveitis can present as.
a) Choroidal tubercleseClinically choroidal tubercle ap-
pears as multiple small nodular lesions that may be
unilateral or bilateral. They are found mostly in
the posterior pole and may have an associated
serous retinal detachment. The tubercles can
sometimes grow into a single mass lesion called
tuberculoma.
b) ChoroidaltuberculomaeChoroidal tuberculomas pre-
sent as a yellowish, subretinal mass and usually have an Fig. 5 e Fundus photo of a patient with TB choroiditis.

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c) Polymerase chain reaction (PCR)eThis technique amplifies

even very small portion of predetermined target region of
Mycobacterium tuberculosis complex DNA. It uses a specific
automated system which can detect as few as one organ-
ism in the fluid such as aqueous or vitreous tap.

3.3. Ancillary investigations20,25e27

a) Mantoux skin teste5 Tuberculin units of purified protein

derivative (PPD) is injected intradermally on the volar
aspect of the forearm and the diameter of induration is
measured (perpendicular to the long axis across the fore-
arm) after 48e72 hrs. An induration of> 10 mm is consid-
ered positive especially in patients living in endemic areas
or high risk individuals.
b) Chest radiographyeThe chest radiograph provides evi-
dence of active infection and healed/primary or reactivated
tubercular lesions. High resolution computerized tomog-
Fig. 6 e Inferior vasculitis with NVD and vitreous
raphy is considered superior to chest radiography espe-
haemorrhage in TB vasculitis.
cially in patients in whom systemic TB is suspected.
c) Interferon gamma release assay (IGRA)eThis test uses
specific genomic region present in Mycobacterium tubercu-
3. Diagnosis and management
losis, ESAT-6 (early secretory antigenic target-6) and CFP-
10(Culture filtrate protein 10). These protein stimulate
There is limited uniformity in the diagnostic criteria for
helper T cell which result in secretion of interferon gamma
intraocular tuberculosis, and it is also difficult to confirm the
which is measured using an Enzyme Linked Immunosor-
diagnosis by laboratory methods.
bent Assay(ELISA).
d) Ocular Imaging: Fluorescein angiography is commonly
3.1. Routine blood investigations used in cases of suspected posterior uveitis due to TB
especially to assess choroidal tubercles. Other imaging
Routine blood investigations like Complete blood count (CBC) studies like ICG angiography, optical coherence tomogra-
and erythrocyte sedimentation rate (ESR) often may not yield phy (OCT), ultrasonography, and ultrasound bio-
any specific diagnosis, but they should be advised in all pa- microscopycan also be used. Indocyanine green
tients. Raised white blood cell count is often seen in patients angiography helps in the detection of subclinical choroidal
with tuberculosis. lesions in patients suspected to have intraocular TB. OCT
helps to evaluate choroidal neovascular membrane for-
mation and cystoid macular edema. Ultrasonography
3.2. Direct investigations20,23e25
helps to localize choroidal tubercles especially in cases
with hazy media and also to differentiate these lesions
a) Microscopy and culture and sensitivityeFor definitive
from any intraocular malignancy.
diagnosis of ocular TB,Mycobacterium tuberculosis organism
in ocular tissues or fluids should be confirmed either by
using histological methods or microbiological in-
vestigations. The microscopic identification for acid fast 4. Medical management20,28e32
bacilli can be performed on the aqueous or vitreous sample
smears using the ZeihleNeelson or fluorescent staining The treatment of tuberculosis is complex and appropriate
techniques. Polymerase chain reaction (PCR) technique can management is required to prevent life threatening
be used to demonstrate the antigens in the various ocular complications.
tissues. The cultures of M. tuberculosis on Lowenstein- Guidelines for diagnosis and management of intraocular
Jenson (egg-based LJ) medium are incubated for a mini- Tuberculosis. (Gupta and Gupta)20:
mum of 8 weeks and the colonies are stained and
confirmed by Ziehl-Neelson stain.
b) BiopsyeDemonstration of granuloma, langerhan's giant
cells, acid fast bacilli in biopsy specimen which is gener- 5. Intraocular tuberculosis
ally taken from easily accessible sites like eyelid, con-
junctiva, lacrimal glands, and chorioretinal biopsy can be - One or more of the clinical signs (A) and one of the positive
diagnostic. tests (B) could be confirmatory for intraocular TB.

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- Any one or more of the clinical signs (A), with any of the agents are rifabutin, fluoroquinolones, interferon-g and
positive tests(C), or a positive therapeutic trial (D) should be linezolid.
presumed to have ocular TB
5.1. Side effect of anti TB drugs
They should get antitubercular therapy provided other
causes of infectious uveitis have been ruled out. - Liver function tests and renal functions need to be moni-
tored in patients on ATT.
A. Clinical signs: - Pyrazinamide is hepatotoxic and causes hyperuricemia.

Celluar reaction in the anterior chamber/vitreous - Rifampin may lead to increase in the clearance of several
with or without posterior synechiae. drugs such as warfarin, corticosteroids, ketoconazole,

Snowball opacities in the inferior vitreous cyclosporine, oral hypoglycaemic agents and protease

Perivascular cuffing of inflammatory exudates inhibitors.

Solitary or multiple granulomas with/without - Rifampin has additive impact on the action of neuromus-
exudative retinal detachment cular blocking agents.

Subretinal abscess - Isoniazid is hepatotoxic and can cause a peripheral neu-

Optic disc granuloma with/without neuroretinitis ropathy which can be inhibited by the intake of 50 mg of
B. Ocular investigations: pyridoxine.

Demonstration of AFB/culture of M. Tuberculosis from - Ethambutol is known to cause optic neuritis, red-green
ocular fluids dyschromatopsia, scotomas, disk edema, disk hyper-

Positive PCR from the ocular fluids to conserved se- emia, peripapillary splinter haemorrhages, and optic
quences of M. Tuberculosis atrophy.
C. Systemic investigations:

Positive Mantoux reaction

Chest radiography suggestive of active/healed TB 6. Steroids in ocular tuberculosis

Evidence of extra-pulmonary TB
D. Therapeutic test - Systemic steroids used for the first few weeks can be used

A positive response to antitubercular therapy over a with antitubercular treatment to decrease damage caused
period of 4e6 weeks. to ocular tissues. However, use of steroids alone should be
avoided as it can flare up systemic tuberculosis and acti-
Ocular TB is treated as other forms of extrapulmonary TB. vate latent lesions.
The treatment requires a bactericidal drug and a sterilizing - Topical steroids are used in the treatment of phlyctenular
agent. The first line anti-tubercular agents are isoniazid, Keratoconjunctivitis, episcleritis, scleritis, interstitial
rifampicin, pyrazinamide, streptomycin and ethambutol. The keratitis and uveitis. Prednisolone acetate eye drops have
recommended doses for treatment of tuberculosis are: good anti-inflammatory effect as compared to other prep-

Daily dose
Drug Children Adult Route Maximum daily dose
Isoniazid 10e20 mg/kg 5 mg/kg Oral/IM 300 mg
Rifampicin 10e30 mg/kg 10 mg/kg Oral 600 mg
Pyrazinamide 15e30 mg/kg 15e30 mg/kg Oral 2 gm
Streptomycin 20e40 mg/kg 15 mg/kg Intramuscular 1 gm
Ethambutol 15e25 mg/kg 15e25 mg/kg Oral 2.5 gm

arations. Periocular steroids are indicated in moderate to

The centre for disease control (CDC) recommends the use severe chronic uveitis, posterior scleritis or recalcitrant
of all four drugs (isoniazid, rifampicin, pyrazinamide, ande- anterior uveitis.
thambutol) for an initial 2-months period followed by a choice - There maybe worsening of inflammation following ATT use
of different options over next 4e7months for the treatment of in patients which may not be controlled with steroids. In
Tuberculosis. such patients immunosuppressants may be added provided
Factors like poor compliance, improper drug regimen, or HIV and other immunosuppressive conditions are ruled out.
natural mutations may play a role in the development of
drug-resistant tuberculosis. The use of multiple second like To provide symptomatic relief from pain and formation of
agents, with a minimum of three orfour additional anti- posterior synechiae adjuvant medical therapy in the form of
tubercular drugs for 18e24 months is advised in multiple cycloplegics and non-steroidal anti-inflammatory drugs
drug resistant tuberculosis (MDR-TB). The additional should be given.

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 i n d i a n j o u r n a l o f t u b e r c u l o s i s x x x ( 2 0 1 5 ) 1 e8 7

in developing countries. This review highlights the clinical

7. Differential diagnosis of ocular manifestations, laboratory diagnosis, and the current diag-
tuberculosis nostic criteria that would help in the management of pre-
sumed or confirmed ocular tuberculosis.
The conditions that can mimic ocular TB are:

Conflicts of interest
Infectious disorders Non-infectious disorders
Syphilis Sarcoidosis All authors have none to declare.
Toxoplasmosis Behcet's disease
Toxocariasis
Candidiasis Metastasis
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