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ARTICLE

Cataract formation associated with ocular


toxocariasis
Seong Joon Ahn, MD, Se Joon Woo, MD, PhD, Joon Young Hyon, MD, Kyu Hyung Park, MD, PhD

PURPOSE: To report the clinical features of cataracts in eyes with ocular toxocariasis.
SETTING: Department of Ophthalmology, Seoul National University Bundang Hosptal, Seongnam,
South Korea.
DESIGN: Retrospective observational case series.
METHODS: The clinical diagnosis of ocular toxocariasis was based on the following characteristic
features: retinal granuloma with or without ocular inflammation and positive results in serum
antibody enzyme-linked immunosorbent assay. Patients younger than 60 years who presented with
a unilateral cataract and were diagnosed with ocular toxocariasis between January 2009 and January
2012 were included. Demographic and ocular examination data for all patients showing atypical
cataract features were collected. All cataracts were documented with anterior segment photography.
RESULTS: Seven of 83 patients (8.4%) presented with an atypical cataract in the eye with ocular
toxocariasis only. The mean patient age was 49.7 years G 8.3 (SD) (range 38 to 59 years). All
patients had small, round, white lens opacities resembling retinal granulomas. The granulomalike opacities were located primarily in the lens midperiphery and in the subcapsular level. The
lens opacity migrated in 1 patient.
CONCLUSIONS: Ocular toxocariasis can cause a cataract with distinctive clinical features. These
cataracts show a granuloma-like opacity primarily in the posterior subcapsular level; the opacity
can migrate.
Financial Disclosure: No author has a financial or proprietary interest in any material or method
mentioned.
J Cataract Refract Surg 2013; 39:830835 Q 2013 ASCRS and ESCRS

Cataracts associated with infections have been reported in several studies. Most studies report infectious
agents as the cause of congenital cataracts15 and a few
reports present adult cases of infection-associated cataract.68 These studies have also shown that the cataracts
are caused by toxoplasmosis, rubella, cytomegalovirus,

Submitted: October 16, 2012.


Final revision submitted: December 14, 2012.
Accepted: December 15, 2012.
From the Department of Ophthalmology, Seoul National University
College of Medicine, Seoul National University Bundang Hospital,
Seongnam, South Korea.
Corresponding author: Se Joon Woo, MD, PhD, Department of
Ophthalmology, Seoul National University Bundang Hospital,
#300, Gumi-dong, Bundang-gu, Seongnam, Gyeonggi-do
463-707, South Korea. E-mail: sejoon1@snu.ac.kr.

830

Q 2013 ASCRS and ESCRS


Published by Elsevier Inc.

herpes simplex virus, syphilis by Treponema pallidum,


Taenia solium, and Mycobacterium leprae.
Toxocariasis is caused by Toxocara canis and Toxocara cati, 2 common species of intestinal roundworm
in dogs and cats.9,10 Toxocara eggs accidentally ingested via soil or contaminated food hatch in the small
intestine. The larvae then penetrate the intestinal wall,
enter the circulation, and migrate to multiple organs.
The resulting conditions may include visceral larva
migrans, cutaneous larva migrans, and ocular larva
migrans, depending on the involved organs.9,10 Ingestion of larvae encapsulated in raw tissues of paratenic
hosts (eg, cows, sheep, and chicken) is another transmission route of Toxocara infection. Despite being
1 of the most prevalent human helminth infections
worldwide, the magnitude and impact of this disease
are not well known by the public.9,10
The clinical features of Toxocara uveitis have been reported in numerous case series.11,12 Although several
0886-3350/$ - see front matter
http://dx.doi.org/10.1016/j.jcrs.2012.12.033

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CATARACT IN OCULAR TOXOCARIASIS

studies report cataract development in patients with


ocular toxocariasis,11,12 the clinical features of these
cataracts have not been well described. We report
7 cases of cataract in middle-aged patients with ocular
toxocariasis, including 6 with active intraocular inflammation and 1 without active inflammation. Our
findings suggest that Toxocara infection is associated
with cataract formation in adults.
PATIENTS AND METHODS
A retrospective chart review was performed for consecutive
adult patients diagnosed with ocular toxocariasis between
January 2009 and January 2012. The Institutional Review
Board of Seoul National University Bundang Hospital
reviewed and approved the study.
Ocular toxocariasis was diagnosed on the basis of typical
clinical features described in previous studies as follows: retinal granuloma with or without intraocular inflammation
and positive results of serum antibody enzyme-linked
immunosorbent assay (ELISA).9,11 Figure 1 shows a typical
presentation of retinal granuloma in ocular toxocariasis.
Patients younger than 60 years and having a unilateral
cataract with an atypical appearance in the eye with ocular
toxocariasis were included in this study.
Demographic and ocular data were collected, including
ocular inflammation status judged according to the standardization of uveitis nomenclature working group's grading scheme,13 features of retinal granuloma, description of
lens opacity, corrected distance visual acuity (CDVA) values,
and visual symptoms. Anterior segment photographs were
also reviewed to evaluate the location of the cataract and
the morphologic features of the lens opacity. In Case 1,
who had a migrating cataract, serial anterior segment photography was performed. Continuous data are presented
as the mean G standard deviation.

Figure 1. Fundus photograph of the right eye of Case 7. A typical


retinal granuloma in ocular toxocariasis is visible and appears as
a small, round, white opacity in the posterior pole.

RESULTS
Of the 83 patients with unilateral ocular toxocariasis
who were younger than 60 years, 7 (8.4%) were included in this study. These 7 patients (4 men, 3 women)
had granuloma-like opacities that closely resembled
retinal granulomas in appearance in the eye affected
by ocular toxocariasis. Table 1 shows the clinical
characteristics of the included patients. The mean
age at cataract presentation was 49.7 G 8.3 years
(range 38 to 59 years). No patient had a history of
diabetes mellitus, and 2 patients had hypertension.
None of the patients had a history of ocular trauma.
All patients with unilateral ocular toxocariasis had
atypical lens opacities only in the eye affected by ocular

Table 1. Clinical characteristics of patients who were clinically and serologically diagnosed with ocular toxocariasis. Morphologic features
of the cataracts are also provided.

Case (Figure)

Age (Y) Sex Location

1 (Figure 3)

54

2 (Figure 2, A)

52

3 (Figure 2, B)

38

4 (Figure 2, C)

55

5 (Figure 2, D)

59

6 (Figure 2, E)

52

7 (Figures 1, 2, F)

38

PSC

Morphology of
Lens Opacity

Granuloma-like
opacity
PSC
Granuloma-like
opacity
PSC
Granuloma-like
opacity
PSC
Granuloma-like
opacity
PSC
Granuloma-like
opacity with linear
tail-like extension
ASC
Granuloma-like
opacity
Capsular
Granuloma-like
opacity

CDVA

Serum Antibody
ELISA

20/20

Positive

20/40

Positive

20/22

Positive

20/40

Positive

20/25

Positive

20/30

Positive

20/400

Positive

Funduscopic
Feature

Uveitis

Visual
Symptom

Posterior pole
Anterior
None
granuloma
Posterior pole
Anterior
Blurred
granuloma
vision
Posterior pole
None
Paracentral
granuloma
scotoma
Peripheral
Intermediate
Blurred
granuloma
vision
Peripheral
Intermediate
Floater
granuloma
Peripheral
Intermediate
None
granuloma
Posterior pole Panuveitis Vision loss
granuloma

ASC Z anterior subcapsular; CDVA Z corrected distance visual acuity; ELISA Z enzyme-linked immunosorbent assay; Granuloma-like opacity Z small,
round, white opacity in the lens; PSC Z posterior subcapsular

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CATARACT IN OCULAR TOXOCARIASIS

Figure 2. Anterior segment photographs show a granuloma-like


lens opacity in eyes with ocular
toxocariasis. A: Case 2. B: Case 3.
C: Case 4. D: Case 5. E: Case 6.
F: Case 7. A through D show posterior subcapsular cataracts. E shows
a small round anterior subcapsular
opacity, and F shows capsule
opacities (arrows).

toxocariasis. Figure 2 shows anterior segment photographs of these eyes. Cataracts associated with ocular
toxocariasis were generally similar in appearance and
were small (!3.0 mm), round, and white. The opacities
closely resembled the retinal granulomas observed in ocular toxocariasis. The most common type of cataract in
patients with ocular toxocariasis was posterior subcapsular (5 eyes). A capsular cataract and anterior subcapsular cataract were noted in 1 patient each. The CDVA
varied between 20/400 and 20/20, but most eyes (6 of
7) had a CDVA of 20/40 or better. Case 7 showed profound vision loss (20/400 on Snellen chart), which
most likely resulted from diffuse intraocular inflammation. The patient's CDVA improved to 20/30 after the intraocular inflammation was controlled with a topical
corticosteroid. One eye (Case 1) had migration of the
lens opacities over a relatively short period (4 months).
Case 1
A 54-year-old man with a medical history significant only for hypertension presented with

conjunctival injection and ocular pain in the left eye;


these symptoms had begun 10 days previously. The
CDVA was 20/20 in the right eye and 20/40 in the
left eye. Slitlamp examination showed keratic precipitates and grade 0.5C inflammation in the anterior
chamber of the left eye (1 to 5 cells in a 1.0 mm 
1.0 mm slit beam under maximum light intensity).
An anterior segment photograph showed a posterior
subcapsular cataract presenting as 2 granuloma-like
white opacities in the lens midperiphery (Figure 3, A).
On the basis of the presence of a posterior pole granuloma, identified by indirect ophthalmoscopy, and
a positive serum Toxocara ELISA result, the patient
was diagnosed with ocular toxocariasis in the left
eye. Ocular inflammation was controlled with topical
prednisolone acetate 1%, instilled 4 times a day, and
homatropine 2%, used twice a day. Four months after
the diagnosis, the CDVA improved to 20/30, and the
2 granuloma-like white opacities had migrated
centrally and merged into 1 larger, granuloma-like
opacity (Figure 3, B).

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CATARACT IN OCULAR TOXOCARIASIS

Figure 3. Anterior segment photographs from Case 1 at the initial


visit (A) and 4 months later (B). Arrows indicate granuloma-like
lens opacities. Compared with the initial visit, the opacities were
more centrally located and 1 larger opacity had formed from the
merging of the 2 granuloma-like opacities.

DISCUSSION
Our understanding of ocular toxocariasis is poor
because of insufficient clinical awareness.9 In particular, cataract development in ocular toxocariasis has
been reported in very few case series11,12 and clinical
features of the cataracts have not been adequately elucidated. In this report, we found that the morphology
of the lens opacity in ocular toxocariasis was similar to
that of a retinal granuloma.
Stewart et al.11 report 3 cases of ocular toxocariasis
(12.5% of all cases) in which cataract had developed,
and a posterior subcapsular cataract was reported in
an eye with ocular toxocariasis.14 Woodhall et al.12
also showed that cataracts are the second most common indication for surgical treatment (3 patients
treated with cataract surgery) in patients with ocular
toxocariasis. In a study of the outcomes of cataract

833

extraction in eyes with uveitis by Kawaguchi et al.,15


toxocariasis was present in 2 (1.5%) of 131 cases. Of
83 ocular toxocariasis patients younger than 60 years,
7 (8.4%) developed lens opacities with characteristic
features in our study. A unilateral granuloma-like
lens opacity developed in the eye affected by ocular
toxocariasis. Posterior subcapsular cataract was the
most common type of cataract in these eyes, and
most cataracts were not visually significant.
It is unclear whether ocular toxocariasis was the true
cause of cataract in these cases. Other possible causes
could be aging, uveitis, corticosteroid use, and/or systemic disease, such as diabetes mellitus. However, in
our cases, the effect of corticosteroid and systemic
factors was considered insignificant. Although the appearance of the cataracts in eyes treated with a topical
corticosteroid, that is granular areas or plaque in the
posterior subcapsular cortex,16,17 is similar to the
appearance in our cases, the cataracts were identified
before steroid treatments were initiated in our cases
and no patient had been diagnosed with diabetes mellitus. All patients in our case series were younger than 60
years and showed unilateral involvement in the eye
with ocular toxocariasis; thus, age-related cataractogenesis was not strongly suspected. In addition, 7 patients
had a nearly identical presentation and the lens opacity
morphology was similar to the typical retinal granuloma morphology in eyes with ocular toxocariasis.
Thus, our observations suggest that cataract formation
was associated with ocular toxocariasis in our patients.
The correlation between clinical appearance and
histopathology is important for understanding the
association between cataract formation and ocular toxocariasis. We did not perform histologic examination
because our patients had visually insignificant cataracts and had therefore not had cataract extraction;
however, several possible mechanisms of cataract formation in eyes with ocular toxocariasis can be suggested from earlier reports of the histopathology of
cataracta complicata and a clinicopathologic study of
ocular toxocariasis. Bartz-Schmidt et al.18 found an
inflammatory pathogenesis of cataract formation,
namely, granulomatous inflammatory infiltrate, in an
eye with herpes keratouveitis. Another theory for the
cataracta complicata in anterior uveitis is the deposition of pathological material from the aqueous humor
into the lens capsule.19 However, Eshagian et al.16
found disorganized lens fibers in an eye with cataracta
complicata that showed plaque-like or snowball
opacity. Of the clinicopathologic reports on ocular
toxocariasis, Werner et al.20 showed degenerated larval structures within the central area of necrosis and
granulomatous inflammation in the retinal lesion.
Based on the findings in these reports, 3 possible mechanisms can be proposed for cataract formation in our

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CATARACT IN OCULAR TOXOCARIASIS

patients: granulomatous inflammation, deposition of


pathological material from the aqueous humor, and
disorganized lens fibers. Inflammation was noted in
the anterior chamber in patients with smaller anterior
dot-like opacities (Cases 6 and 7), suggesting that the
deposition of pathological material from the aqueous
humor in the anterior part of the lens was the possible
mechanism in these cases. In cases with larger posterior granuloma-like opacities, granulomatous inflammation may be a more probable cause of lens opacity
and disorganized lens fibers may be another underlying pathology. In particular, the lens opacity migration
that occurred in Case 1 suggests that the lens lesion
was caused by Toxocara larvae, which showed intraocular migration in previous reports.21,22 To confirm the
association between granuloma-like lens opacity and
ocular toxocariasis, histologic examination of the lens
lesions may be helpful.
In summary, a cataract can develop in eyes with
ocular toxocariasis and typically presents as a posterior
subcapsular granuloma-like opacity. The knowledge
that cataracts are a possible manifestation of ocular
toxocariasis may aid in the clinical diagnosis of the disease. In addition, Toxocara is likely an infectious agent
that can cause cataract development in adult patients.
Although visual axis opacification was uncommon in
our case series, these cataracts should be carefully
monitored because of the risk for migration.
WHAT WAS KNOWN
 Ocular toxocariasis is a well-defined disease entity, and
its typical presentations are retinal granuloma and ocular
inflammation.
 Although several case series have reported cataracts in
eyes with ocular toxocariasis, the morphologic features
of the cataracts and their incidence have not been well
described.
WHAT THIS PAPER ADDS
 Approximately 8% of eyes with ocular toxocariasis had
distinctive cataracts with granuloma-like opacities mostly
at the posterior subcapsular level.
 In eyes with ocular toxocariasis, the cataract was usually
visually insignificant but the lens opacity might migrate;
therefore, careful follow-up examinations are required.

REFERENCES
1. Arun V, Noble AG; other members of the Toxoplasmosis Study
Group. Cataracts in congenital toxoplasmosis. J AAPOS 2007;
11:551554

2. Eckstein M, Vijayalakshmi P, Killedar M, Gilbert C, Foster A.


Aetiology of childhood cataract in south India. Br J Ophthalmol
1996; 80:628632. Available at: http://www.ncbi.nlm.nih.gov/pmc/
articles/PMC505557/pdf/brjopthal00007-0048.pdf. Accessed
January 12, 2013
3. Eckstein MB, Brown DWG, Foster A, Richards AF, Gilbert CE,
Vijayalakshmi P. Congenital rubella in south India:
diagnosis using saliva from infants with cataract. BMJ 1996;
312:161. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/
PMC2349853/pdf/bmj00525-0033.pdf. Accessed January 12,
2013
4. Raghu H, Subhan S, Jose RJ, Gangopadhyay N, Bhende J,
Sharma S. Herpes simplex virus-1-associated congenital cataract. Am J Ophthalmol 2004; 138:313314
5. Mahalakshmi B, Therese KL, Shyamala G, Devipriya U,
Madhavan HN. Toxoplasma gondii detection by nested polymerase chain reaction in lens aspirate and peripheral blood leukocyte in congenital cataract patients: the first report from
a tertiary eye hospital in India. Curr Eye Res 2007; 32:653657
6. Adegbehingbe BO, Soetan EO, Adeoye AO. Case report: intraocular cysticercosis. West Afr J Med 2003; 22:354355. Available at: http://www.ajol.info/index.php/wajm/article/download/
28064/21853. Accessed January 12, 2013
7. Brandt F, Kampik A, Malla OK, Pokharel RP, Wos J.
Blindness from cataract formation in leprosy. Dev Ophthalmol
1983; 7:112
8. Courtright P, Lewallen S, Tungpakorn N, Cho B-H, Lim Y-K,
Lee H-J, Kim S-H. Cataract in leprosy patients: cataract surgical
coverage, barriers to acceptance of surgery, and outcome of
surgery in a population based survey in Korea. Br J Ophthalmol
2001; 85:643647. Available at: http://www.ncbi.nlm.nih.gov/
pmc/articles/PMC1723998/pdf/v085p00643.pdf.
Accessed
January 12, 2013
9. Rubinsky-Elefant G, Hirata CE, Yamamoto JH, Ferreira MU. Human toxocariasis: diagnosis, worldwide seroprevalences and
clinical expression of the systemic and ocular forms. Ann Trop
Med Parasitol 2010; 104:323
10. Smith H, Holland C, Taylor M, Magnaval J-F, Schantz P,
Maizels R. How common is human toxocariasis? Towards standardizing our knowledge. Trends Parasitol 2009; 25:182188
11. Stewart JM, Cubillan LDP, Cunningham ET Jr. Prevalence, clinical features, and causes of vision loss among patients with ocular toxocariasis. Retina 2005; 25:10051013
12. Woodhall D, Starr MC, Montgomery SP, Jones JL, Lum F,
Read RW, Moorthy RS. Ocular toxocariasis: epidemiologic, anatomic, and therapeutic variations based on a survey of ophthalmic subspecialists. Ophthalmology 2012; 119:12111217
13. The Standardization of Uveitis Nomenclature (SUN) Working
Group. Standardization of uveitis nomenclature for reporting
clinical data. Results of the First International Workshop. Am J
Ophthalmol 2005; 140:509516
14. Shields JA, Parsons HM, Shields CL, Shah P. Lesions simulating retinoblastoma. J Pediatr Ophthalmol Strabismus 1991;
28:338340
15. Kawaguchi T, Mochizuki M, Miyata K, Miyata N. Phacoemulsification cataract extraction and intraocular lens implantation in patients with uveitis. J Cataract Refract Surg 2007; 33:305309
16. Eshagian J, Rafferty NS, Goossens W. Human cataracta complicata; clinicopathologic correlation. Ophthalmology 1981;
88:155163
17. Vasavada AR, Mamidipudi PR, Sharma PS. Morphology of and
visual performance with posterior subcapsular cataract.
J Cataract Refract Surg 2004; 30:20972104
18. Bartz-Schmidt KU, Hartmann C, Kirchhof B, Krieglstein GK. Zur
Genese der Cataracta complicata bei herpetischer Keratouveitis

J CATARACT REFRACT SURG - VOL 39, JUNE 2013

835

CATARACT IN OCULAR TOXOCARIASIS

[Pathogenesis of complicated cataract in herpetic keratouveitis].


Klin Monatsbl Augenheilkd 1996; 209:228231
19. Seland JH. The ultrastructure of the human lens capsule. II. Cataracta complicata; a transmission electron microscopic study.
Acta Ophthalmol (Copenh) 1978; 56:723734
20. Werner JC, Ross RD, Green WR, Watts JC. Pars plana
vitrectomy and subretinal surgery for ocular toxocariasis. Arch
Ophthalmol 1999; 117:532534. Available at: http://archopht.
jamanetwork.com/data/Journals/OPHTH/9855/ecp8113.pdf.
Accessed January 12, 2013
21. Suzuki T, Joko T, Akao N, Ohashi Y. Following the migration of
a Toxocara larva in the retina by optical coherence tomography
and fluorescein angiography. Jpn J Ophthalmol 2005; 49:159161

22. Sivaratnam D, Subrayan V, Ali NA. Transvitreal migration of


a Toxocara larva resulting in a second chorioretinal granuloma
[letter]. Jpn J Ophthalmol 2008; 52:416417

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First author:
Seong Joon Ahn, MD
Department of Ophthalmology,
Seoul National University Bundang
Hospital, Seongnam, South Korea