MAJOR ARTICLE
Ocular Manifestations Associated with Brucellosis:
A 26-Year Experience in Peru
Isaias Rolando,1,2 Liset Olarte,2 Gustavo Vilchez,2 Marina Lluncor,2 Larissa Otero,2 Mark Paris,4,5 Carlos Carrillo,3
and Eduardo Gotuzzo,1,2
1
Hospital Nacional Cayetano Heredia, 2Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, and
Department of Microbiology, Universidad Peruana Cayetano Heredia, Lima, Peru; and 3Department of Ophthalmoloy, A. G. Holley State Hospital,
Lantana, and 4Florida Department of Health, Tallahasee, Florida
5
Background. Brucellosis has unusual clinical manifestations. Ocular involvement caused by brucellosis remains
poorly recognized in areas in which brucellosis is endemic.
Methods. A prospective study was performed to evaluate patients attending the Instituto de Medicina Tropical
“Alexander von Humboldt” and the Hospital Nacional Cayetano Heredia (Lima, Peru) from January 1980 through
December 2005 who received a diagnosis of brucellosis with ocular involvement. Diagnosis was made on the basis
of clinical findings as well as agglutinations and/or culture positive for Brucella melitensis.
Results. During a period of 26 years, 1551 patients with brucellosis were seen, including 52 patients with
ocular brucellosis. We found that 7 (0.7%) of 965 patients with acute brucellosis and 45 (7.9%) of 570 patients
with chronic brucellosis had ocular brucellosis (P ! .001 ). In 16 patients with brucellosis, the disease stage was
unclassified. The most frequent ocular presentation was uveitis, which was found in 43 (82.7%) of the 52 patients
with ocular brucellosis. Posterior uveitis was the most frequent uveal syndrome (21 cases; 45.7%). Patients with
panuveitis had the worst visual prognosis: 8 of 9 patients with panuveitis were legally blind, including 5 patients
with no light perception.
Conclusions. Brucellosis may involve the eye and can lead to serious complications. In patients with brucellosis,
early ophthalmologic evaluation can lead to prompt treatment and might prevent blindness from severe ocular
damage.
Brucellosis is a zoonotic disease that can be found
worldwide. Although it has been eradicated and is under control in most developed countries, it still represents an important health problem in many parts of
the world, including the Middle East, the Mediterranean, Mexico, and Central and South America [1–3].
In some countries, such as Peru, Kuwait, and Saudi
Arabia, brucellosis is endemic [3, 4].
In the genus Brucella, there are 6 classic pathogens,
4 of which have been recognized as human pathogens:
Brucella melitensis, Brucella abortus, Brucella canis, and
Brucella suis. Most cases in the world are caused by B.
melitensis, which has been described as the most vir-
Received 12 September 2007; accepted 8 December 2007; electronically
published 20 March 2008.
Reprints or correspondence: Dr. Eduardo Gotuzzo, Instituto de Medicina Tropical
“Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Av. Honorio
Delgado 430, Lima 31, Peru ([email protected]).
Clinical Infectious Diseases 2008; 46:1338–45
2008 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2008/4609-0002$15.00
DOI: 10.1086/529442
1338 • CID 2008:46 (1 May) • Rolando et al.
ulent Brucella species [1, 4, 5]. B. abortus is the most
prevalent Brucella species in North America and Europe, whereas B. melitensis is more common in Latin
America, the Mediterranean, and developing countries
[1, 4]. In Peru, Brucella melitensis has been isolated in
all cases in which cultures have been obtained.
Brucellosis is a systemic disease with a wide spectrum
of clinical manifestations, which presents a diagnostic
challenge. Even though classical symptoms of brucellosis are easy to recognize, some presentations are not
well known, such as ocular brucellosis, and have to be
considered when making a differential diagnosis. This
could permit early diagnosis and treatment and, hopefully, reduce the number of complications [6].
The first case of ocular brucellosis in a human being
was described by Lemaire in 1924 [7]. Cases involving
uveitis, neuritis, optic neuritis, papilloedema, keratitis,
and more-diverse ocular and neurological presentations
associated with brucellosis have been reported [8].
With improved quality control of animal products
and adequate livestock vaccination, the number of
Table 1. Incidence of brucellosis and ocular brucellosis, by sex
and clinical course.
Variable
Systemic brucellosis
(n p 1551)
Ocular brucellosis
(n p 52)
P
658
893
18
34
.24
965
570
7
45
!.001
Sex
Male
Female
a
Clinical course
Acute
Chronic
a
Clinical course was undefined for 16 patients.
brucellosis cases has been reduced in developed countries. Reported cases have been scarce, and in general, only anecdotal
reports exist [9]. In those reports, ocular brucellosis has been
described as an unusual presentation of the disease [2, 6, 10].
The aim of this study was to report ocular brucellosis presentations in a clinical series of 11500 patients with brucellosis.
PATIENTS, MATERIALS, AND METHODS
We prospectively included all patients with a diagnosis of systemic brucellosis attending the Instituto de Medicina Tropical
“Alexander von Humbolt” and the Hospital Nacional Cayetano
Heredia (Lima, Peru) from January 1980 through December
2005. We selected all patients with a diagnosis of brucellosis
who had ocular involvement and all patients referred to our
clinic for ocular lesions who were subsequently diagnosed as
having brucellosis.
Patients with a diagnosis of brucellosis received evaluation
by an infectious diseases specialist (E.G.) and a clinical microbiologist (C.C.). When ocular abnormalities were found, patients were referred to an ophthalmologist (I.R.) who systematically observed those patients with ocular involvement.
The inclusion criteria for our study were (1) agglutination
test results positive for Brucella melitensis in blood (serum agglutination titer ⭓1:160, 2-mercaptoethanol titer ⭓1:80, and
blocking antibody titer ⭓1:80) and/or (2) isolation of B. melitensis from blood or bone marrow cultures [11].
Patients with ocular involvement were tested using the Venereal Disease Research Laboratory assay and/or the Fluorescent Treponemal Antibody Absorption assay, and they underwent serological testing for toxoplasmosis. Active tuberculosis
was ruled out by clinical examination, tuberculin skin testing,
and examination of chest radiographs.
Two different clinical courses were recognized for the disease:
acute brucellosis (!8 weeks in duration) and chronic brucellosis
(⭓8 weeks in duration). We considered cases with a subacute
or recurrent course to be cases of chronic brucellosis for the
purpose of simplifying the statistical analysis.
The following presentations of uveitis were identified: (1)
anterior uveitis, including iritis, iridocyclitis, and anterior cy-
clitis; (2) intermediate uveitis, including pars planitis, posterior
cyclitis, and hyalitis; (3) posterior uveitis, including choroiditis,
chorioretinitis, retinitis, and neuroretinitis; and (4) panuveitis,
including inflammation of all 3 components of the uveal tract
[12]. The following complications were identified: cataracts,
glaucoma, maculopathy, vitreal alterations, phthisis bulbi, optic
atrophy, neovascular retinal membrane, tractional retinal detachment, Behcet syndrome, Harada syndrome (posterior uveal
inflammation with retinal exudations and meningeal irritation),
and Vogt-Koyanagi-Harada syndrome (anterior segment inflammation associated with vitiligo, poliosis, disacusia, and meningeal irritation) [13].
All patients received standard therapy with doxycycline (100
mg twice per day for 6 weeks) in combination with rifampin
(600–1200 mg/day for 6 weeks) or an aminoglycoside (administered intramuscularly once per day for 2 weeks), which was
usually streptomycin (15 mg/kg or 1 g per day). If ocular inflammation was present, systemic and topical steroids were also
prescribed for 2–4 weeks.
Data was tabulated in a Microsoft Excel spreadsheet with a
unique identification code for each patient. Variables included
were sex, age, systemic manifestations, and clinical course. In
patients with ocular involvement, we considered ophthalmologic symptoms, initial and final visual acuity, unilateral or
bilateral ocular involvement, uveal presentation, ocular complications, serum agglutination test results, and culture results.
Data were analyzed using Stata, version 7.0 (Stata). For statistical analysis, independent variables were compared using the
x2 test. P ! .05 was considered to be statistically significant.
RESULTS
Fifty-eight of 1551 patients with systemic brucellosis had ocular
involvement. Six of the patients with ocular involvement did
not meet inclusion criteria for this study (5 patients had serum
agglutination titers that were too low for inclusion, and 1 patient had ocular toxoplasmosis). Over a 26-year period, 52
patients with ocular brucellosis were registered; of these, 34
(65.4%) were women, and 18 (34.6%) were men (table 1).
Table 2. Systemic signs and symptoms of patients with ocular
brucellosis.
Systemic sign or symptom
Arthralgias
Fever
No. (%)
of patients
(n p 52)
26 (50)
24 (46.2)
Headache
Sweating
Testicular paina
5 (9.6)
5 (9.6)
3 (16.7)
Asymptomatic
15 (28.8)
a
Three of 18 male patients reported testicular pain.
Ocular Brucellosis • CID 2008:46 (1 May) • 1339
Table 3. Types of ocular involvement in patients with ocular
brucellosis.
Type of ocular involvement
No. (%)
of patients
(n p 52)
Ophthalmologic manifestation
a
Overall
Uveitis
48
b
Overall
43 (82.7)
Anterior uveitis
Posterior uveitis
8
21
Intermediate uveitis
Panuveitis
Keratitis
Conjunctivitis
8
9
3 (5.8)
2 (3.8)
Neuro-ophthalmologic manifestations
Overall
Papilloedema
Papilitis
Third cranial nerve paresis
a
b
7
5 (9.6)
1 (1.9)
1 (1.9)
Three patients had 11 ocular manifestation.
Three patients had different uveal involvement in both eyes.
Thirty-six cases of brucellosis (69.2%) were diagnosed using
serum agglutination titers only. Four cases (7.7%) were diagnosed using only culture results. Diagnosis was made with both
methods in 12 cases (23.1%). Bone marrow and/or blood samples were cultured in 35 cases, and B. melitensis was recovered
in 16 (45.7%). Ocular involvement was reported for 7 (0.7%)
of 965 patients with acute brucellosis, whereas 45 (7.9%) of
570 patients with chronic brucellosis had ocular involvement
(table 1). Among the 52 patients with ocular brucellosis, age
distribution was as follows: 26 (50%) were 16–35 years of age,
14 (26.9%) were 155 years of age, 11 (21.2%) were 36–55 years
of age, and 1 (1.9%) was ⭐15 years of age.
Systemic symptoms were present in 37 cases (71.2%) and
absent in 15 cases (28.8%) (table 2). The most frequent ocular
symptom reported was blurred vision (36 cases [69.2%]), followed by red eyes (9 cases [17.3%]), eye pain (6 cases [7.7%]),
foreign body sensation (3 cases [5.8%]), scotoma in (3 cases
[5.8%]), loss of vision (2 cases [3.9%]), double vision (2 cases
[3.9%]), and lacrimation (1 case [1.9%]). Ten patients (19.3%)
did not present with ocular symptoms but had abnormal findings of ophthalmologic examinations (5 of these 10 patients
had visual acuity impairment).
Unilateral ocular involvement was reported for 32 (61.5%)
of the patients, and bilateral ocular involvement was reported
for 20 (38.5%). Ophthalmologic and neuro-ophthalmologic abnormalities were reported. Forty-three patients (82.7%) had
cases of uveitis; among these patients, the posterior presentation
was the most frequent (21 patients; 45.7%) (table 3).
A total of 56 ocular complications were present in 36 patients
1340 • CID 2008:46 (1 May) • Rolando et al.
(69.2%). Some patients experienced 11 complication, and 16
patients (30.8%) did not have any complications (table 4)
Visual prognosis in patients with ocular brucellosis was based
on visual acuity after treatment. Data on the visual acuity of 2
patients, 1 with anterior uveitis and 1 with intermediate uveitis,
were not available. Eleven of 14 patients with anterior and
intermediate uveitis had a visual acuity better than 20/50 after
treatment; 4 of 21 patients with posterior uveitis and 8 of 9
patients with panuveitis were legally blind after treatment. The
latter group included 5 patients with no light perception. The
worst prognosis was observed for patients with panuveitis and
posterior uveitis (table 5).
DISCUSSION
Since the start of the twentieth century, a number of ocular
presentations associated with brucellosis have been reported
[14, 15]. Nevertheless, there is no data on the incidence of this
pathology, because most citations in the literature refer to case
reports. In this study, ocular involvement due to brucellosis
was reported in 52 (3.4%) of 1551 patients with brucellosis.
Güngür et al. [16] reported that 38 (26%) of 147 patients with
brucellosis had ocular brucellosis. Puig Solanes et al. [8] reported 60 (14.5%) cases out of 413 patients, and Rolando et
al. [17] reported 14 (20%) out of 70 patients.
In this study, a higher proportion of ocular brucellosis was
found in women (65.4%). This is consistent with previous findings by Puig Solanes et al. [8] and Rolando [18], who reported
that 66% and 86.7% of patients with ocular brucellosis were
female, respectively.
Many Peruvian studies of brucellosis report that female patients experience a larger number of symptoms and increased
severity of symptoms [19, 20]. Most clinical studies of uveitis
Table 4. Complications and sequelae of ocular brucellosis.
Complication
Cataracts
Vitreal alterations
No. (%)
of patients
(n p 36)
18 (34.6)
11 (21.2)
Phthisis bulbi
Maculopathy
6 (11.5)
6 (11.5)
Glaucoma
Neovascular retinal membrane
5 (9.6)
3 (5.8)
Harada syndrome
Optic atrophy
3 (5.8)
1 (1.9)
Tractional retinal detachment
1 (1.9)
Behcet syndrome
Vogt-Koyanagi-Harada syndrome
None
1 (1.9)
1 (1.9)
16 (30.8)
NOTE. A total of 56 complications were experienced. Some patients experienced 11 complication.
Figure 1. Ocular presentations associated with brucellosis. A, Phthisis bulbi. B, A and B ultrasound of the patient shown in A. Retinographh (C)
and retinal angiogram (D) with window defect in the retinal pigmentary epithelium secondary to chronic edema in the macular area, showing evidence
of septic emboli in a patient with brucellar endocarditis and focal choroiditis. E, Retinograph showing serous macular retinal detachment secondary
to juxtapapillar choroidal granuloma in a 33-year-old man with chronic brucellosis. F, Retinograph of the patient shown in E, showing juxtapapillary
chorioretinal scar 4.5 years after diagnosis of choroidal granuloma and 3 months of laser treatment. G, Anterior uveitis and secondary cataracts. H,
Blue toluidine stain of iris biopsy sample from the patient shown in G, with granulomatous inflammatory reaction. The presence of Russell bodies
(arrow) is the evidence of local production of specific immunoglobulins.
report a similar incidence in both sexes [21]. Although our
study found that more women than men were affected, the
difference was not statistically significant.
In this study, patients 16–35 years of age were encountered
more frequently than patients in other age groups. This is con-
sistent with the findings of Puig Solanes et al. [8], who found
a higher prevalence of ocular brucellosis among young adults
(21–30 years of age). We had only 1 patient ⭐15 years of age,
whereas 13.3% of the cases reported by Puig Solanes et al. [8]
occurred in patients who were ⭐15 years of age.
Ocular Brucellosis • CID 2008:46 (1 May) • 1341
Table 5. Visual prognosis of uveitis.
Anterior
uveitis
(n p 7)
Intermediate
uveitis
(n p 7)
Posterior
uveitis
(n p 21)
Panuveitis
(n p 9)
Total
a
(n p 44)
20–40
50–200
6
1
5
1
11
6
0
1
22
9
400–LP
NLP
0
0
1
0
2
2
3
5
6
7
Visual acuity
NOTE. LP, light perception; NLP, no light perception.
a
Visual acuity was not obtained for 2 patients.
Ocular presentations of brucellosis can appear in either the
acute phase or the chronic phase of the disease. In this study,
a larger proportion of ocular manifestations was found in the
chronic phase (P ! .001) (figure 1A–G). This is consistent with
other reports, such as that by Woods [22], who described ocular
brucellosis only in the chronic phase of the systemic disease.
Rolando et al. [23] and Puig Solanes et al. [8] concluded that
uveitis develops more frequently in individuals with the subacute and chronic forms of brucellosis. Güngür et al. [16] also
found that ocular brucellosis was more frequent during the
chronic phase of the disease (accounting for 71% of cases of
ocular brucellosis). In 1985, Rolando et al. [18] found that 4
(26.7%) of 15 patients presented during the acute phase of the
disease, whereas 11 (73.3%) presented during the chronic and
undulating phase. Moreover, Green [14], reporting on the work
of 23 authors, stated that all ocular compromise appeared during the chronic phase of the systemic disease.
Many factors influence the presentation of ocular compromise during the chronic phase of brucellosis. In developing
countries, patients frequently do not seek medical care until
the disease has reached an advanced stage, and limited knowledge of disease pathology by health care providers often results
in a late diagnosis.
We observed 2 types of ocular involvement: ophthalmologic
and neuro-ophthalmologic. Of the ophthalmologic pathology
caused by Brucella species, the most frequent form that we
encountered was uveitis. It has been recognized as an important
manifestation in ocular brucelosis [24] and widely described
as being the most common form of ocular brucellosis [8, 25–
28]. Only rarely do studies report another presentation as being
Figure 2. Choroidal neovascular membrane. A, Black and white retinal image before contrast with extensive macular edema from the patient shown
in figure 1E and 1F. B, C, and D, Retinal angiogram showing intermediate and late-phase serous macular detachment secondary to choroidal neovascular
membrane (arrow) in a juxtapapillary chorioretinal scar. After 9 weeks of laser treatment, visual acuity improved to 20/20.
1342 • CID 2008:46 (1 May) • Rolando et al.
Figure 3. Retinal detachment in a 59-year-old woman with a paravertebral abscess and classic dorsal brucellar spondylitis. A, A and B
ultrasound of the right eye showing total serous retinal detachment. When
systemic steroids were discontinued, a relapse of the retinal detachment
occurred (B). Retinopexy with a 360–silicon band achieved definitive anatomical reattachment (C). Serum agglutination titer was 1:2560, and 2mercaptoethanol in aqueous humor titer was 1:20. B. melitensis was
isolated from a bone marrow culture.
the most frequent. In a 38-case series of ocular brucellosis,
Güngür et al. [16] described 26 cases of conjunctivitis (68.4%).
According to Woods [29] and Rolando [30], the host-pathogen interaction of humans and Brucella species occurs through
2 mechanisms: direct invasion of the ocular tissue by the microorganism, producing septic emboli to the uveal tissue (figure
1C–D, which shows the evidence of septic emboli in a patient
with brucellar endocarditis and focal choroiditis); and formation of immunoglobulin and circulating immune complexes
(figure 1H) [30, 31]. Improvement in visual acuity with systemic steroids supports the concept that ocular manifestations
of brucellosis have an immune component [32].
The most frequent uveal syndrome was posterior uveitis,
followed by panuveitis. This is consistent with findings reported
by Rolando et al. [23], who found that 9 (35%) of 25 patients
with brucellosis had cases of posterior uveitis (35%), and 8
(32%) had cases of panuveitis.
The compromise of the optic nerve and of cranial nerves
involved in ocular movements has been previously described
in association with brucellosis [8, 25]. These neuro-ophthalmologic cases represent a small proportion of our cases. However, Puig Solanes et al. [8] reported 48 cases of neuro-ophthalmologic brucellosis in a 60-patient series. Most of the
literature on neuro-ophthalmologic involvement in brucellosis
consists of isolated case reports [8, 33–35]. Nevertheless, a study
has reported a frequency of optic nerve involvement of 10.7%
[25].
Optic nerve compromise is believed to be secondary to transient meningeal inflammation. Other studies have suggested
that changes to the optic nerve follow an axonal degeneration
secondary to inflammation caused by brucellosis [8, 33]. These
studies also mention the possibility of ischemic and vasculitic
factors, because visual acuity improvement was found after
steroid treatment. This might be mediated through immune
complexes [8, 33].
Etiological diagnosis of brucellosis is confirmed through the
isolation of the microorganism. A positive culture result is more
frequent in acute cases [26]. The tryptic soy broth (Ruiz-Castañeda biphasic medium) is of great importance for isolation
of brucella, although it requires up to 6 weeks for the microorganism to grow. Isolation rates are greatly increased when
this medium is used [20]. Brucella species grow faster when
cultured from bone marrow aspiration samples, which is consistent with the fact that the bacteria localizes itself in the phagocytic cells of the reticuloendothelial system organs [36].
New techniques have been developed, such as PCR, that are
fast and have a high specificity and sensitivity [37–39]. These
techniques, combined with serological testing, can be used in
any phase of the disease [38]. Still, no standardized diagnosis
for brucellosis has been established [37]. In addition, PCR has
been described as useful for testing samples of fluids other than
blood [5]. To date, there are no reports of PCR used to test
ocular fluids.
Complications of ocular brucellosis can occur [23]. We found
a high proportion of cataracts, followed by vitreal alterations,
phthisis bulbi, maculopathies, glaucoma, neovascular retinal
membrane (figure 2), tractional retinal detachment (figure 3),
and other less frequent complications. In other reports, cataOcular Brucellosis • CID 2008:46 (1 May) • 1343
racts, glaucoma, and maculopathies have been described as
being the most frequent complications of uveitis [40]. Recent
studies have demonstrated that these 3 complications are the
main causes of different levels of visual loss [40]. Therefore,
early diagnosis of ocular manifestations of brucellosis has to
be emphasized. In our study, only 16 patients did not develop
complications. This stresses the importance of an ophthalmologic evaluation in patients with ocular brucellosis.
With regard to the visual prognosis of uveitis, we found worse
acuity in patients with cases of panuveitis and posterior uveitis.
Rolando et al. [23] reported that panuveitis cases were associated with a poor prognosis, compared with cases of anterior
uveitis, which had a better prognosis. In our series, 13 of 52
patients lost vision, which emphasizes the importance of brucellosis as a cause of blindness in areas of endemicity [33].
This prospective study has some limitations. The study design did not allow for follow-up of all patients; only those
patients with ocular involvement had ophthalmic follow-up.
Patients who may have later developed ocular involvement may
have been missed. In addition, it is possible that many cases
of ocular brucellosis might not have been included as a result
of not complying with the inclusion criteria. These cases mainly
occurred in patients with ocular involvement and associated
low agglutination titers (⭐1:80).
We can conclude from this study that the most frequent
manifestation of ocular brucellosis is uveitis, with posterior
uveitis being the most frequent type of uveitis. Ocular damage
occurs mainly in the chronic phase of the disease, and brucellosis with ocular involvement is infrequent in children. We
found that 1 (0.003%) of every 300 children with a diagnosis
of systemic brucellosis had ocular involvement. Children rarely
develop the chronic form of the disease.
In conclusion, brucellosis, like tuberculosis, is a clinical condition that may present in any clinical form. There are no key
diagnostic features that may suggest ocular compromise caused
by brucellosis. Thus, complications of ocular brucellosis must
be considered in an area of endemicity, with brucellosis in the
differential diagnosis for patients with infectious uveitis. Every
patient with a diagnosis of systemic brucellosis should undergo
a routine ophthalmologic evaluation, particularly in an area of
endemicity, such as Peru. This could reduce the possibility of
blindness associated with brucellosis.
Acknowledgments
We thank Dr. César Loza, for his assistance with the statistical analysis,
Dr. Luis Izquierdo Vásquez and Dr. Pedro Saenz Rivera, for their support
in the imaging of eye examinations, and Dr. Jean Paul Faure (Hotel Dieu
de Paris, Paris, France), for providing figure 1G.
Potential conflicts of interests. All authors: no conflicts.
1344 • CID 2008:46 (1 May) • Rolando et al.
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