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534 Übersicht

Ocular Toxoplasmosis: an Update


Aktuelles zur okulären Toxoplasmose

Author J. G. Garweg

Affiliation Clinic for Vitreoretinal Diseases and Uveitis, Berner Augenklinik am Lindenhofspital, Swiss Eye Institute, Bern and Rotkreuz,
and University of Bern, Switzerland

Key words Abstract Zusammenfassung


l
" ocular toxoplasmosis
! !
l
" pathophysiology

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Introduction: Although the seroprevalence of Hintergrund: Die Seroprävalenz der Toxoplasmo-
l
" burden of disease
toxoplasmosis has undergone a progressive 50 % se ist in den letzten zwanzig Jahren in Europa und
l
" diagnostics

decline during the past 20 years, the disease re- den USA um 50 % zurückgegangen. Wegen der oft
l
" therapy

l
" prophylaxis mains an economically important health hazard erheblichen organischen Folgeschäden stellt die
l
" review in many countries. Ocular toxoplasmosis (OT) is Infektion in vielen Ländern aber weiterhin ein re-
the most frequent cause of infectious posterior levantes gesundheitsökonomisches Problem dar.
Schlüsselwörter
uveitis, and new insights into its pathophysiology Die okuläre Toxoplasmose (OT) ist die häufigste
l
" okuläre Toxoplasmose

have paved the way for new therapeutic strat- Ursache der infektiösen posterioren Uveitis, wes-
l
" Parasiten‑Virulenz

l
" Epidemiologie egies. halb hier Neues zu Pathophysiologie und thera-
l
" Pathophysiologie Methods: This review summarises recent insights peutischen Optionen berichtet wird.
l
" Krankheits‑Manifestationen into the disease, its clinical manifestations and Methoden: Diese Übersicht basiert auf den in den
l
" krankheitsbedingter Schaden
therapeutic options. The data have been gleaned letzten drei Jahren gewonnenen Erkenntnissen zu
l
" Diagnostik
from a PubMed search, which was conducted in den klinischen Manifestationen und therapeuti-
l
" Therapie
August 2015 using the key term “ocular toxoplas- schen Optionen der OT anhand einer Literatur-
l
" Prophylaxe

mosis”. suche in PubMed mit den Schlüsselwörtern „ocu-


l
" Review

Results: A laboratory confirmation of the diagno- lar“ und „toxoplasmosis“.


sis serves as the basis for estimating the clinical Ergebnisse: Die Bestätigung der klinischen Diag-
burden of OT. This is more severe in South Amer- nose mittels Laboruntersuchungen bietet die Ba-
ica than in Europe, due to the higher incidence of sis für die Einschätzung der Infektions-bedingten
the more virulent New World parasitic strains. It gesundheitlichen Schäden. Diese sind in Europa
is not yet possible to differentiate between ac- deutlich weniger schwerwiegend als in Südame-
quired and congenital cases in most patients. rika infolge der höheren Virulenz der Stämme
Bibliography However, in elderly individuals, clinical manifes- aus der Neuen Welt. Eine Differenzierung zwi-
DOI http://dx.doi.org/ tations of acquired OT are more frequently en- schen angeborener und erworbener Infektion an-
10.1055/s-0041-111821 countered and in atypical forms. Although in- hand von Laboranalysen ist weiterhin nicht mög-
Klin Monatsbl Augenheilkd
flammation may initially be more pronounced in lich. Die erworbene OT zeigt schwerere Verläufe
2016; 233: 534–539 © Georg
Thieme Verlag KG Stuttgart · acquired than in congenital cases of OT, the final als die kongenitale, insbesondere bei älteren oder
New York · ISSN 0023-2165 visual acuity is usually better and the risk of re- immunkompromittierten Personen. Obwohl die
currence lower. Amongst the numerous thera- Entzündungsreaktion bei erworbener OT anfangs
Correspondence
Prof. Dr. med. Justus G. Garweg peutic options, none is clearly superior. In immu- schwerer ist, ist eine bleibende Visusminderung
Clinic for Vitreoretinal Diseases nocompromised individuals and in those with seltener. Keine der verfügbaren Antibiotika-The-
and Uveitis frequent recurrences, prophylactic measures rapien ist den Alternativen eindeutig überlegen,
Berner Augenklinik am Linden-
hofspital, Swiss Eye Institute, should be considered. eine Monotherapie mit Steroiden ohne antibioti-
Bern and Rotkreuz, Conclusion: OT is still a potentially vision-threat- sche Abdeckung ist jedoch kontraindiziert. Eine
and University of Bern ening affection, namely in elderly individuals with Rezidivprophylaxe sollte bei immunkompromit-
Bremgartenstrasse 119
3012 Bern acquired disease and in those patients harbouring tierten Patienten und häufigen Rezidiven erwo-
Switzerland the more aggressive New World strains of the par- gen werden.
Tel.: + 41/31/3 11 12 22 asite. Owing to the limitations in diagnostic sensi- Schlussfolgerung: Die OT sollte als Differenzial-
Fax: + 41/31/3 11 14 33
justus.garweg@ tivity and therapeutic efficacy, treatment strat- diagnose bei atypischer Präsentation einer poste-
swiss-eye-institute.com egies have to be tailored to the individual needs. rioren Uveitis bedacht werden, insbesondere bei

Garweg JG. Ocular Toxoplasmosis: an … Klin Monatsbl Augenheilkd 2016; 233: 534–539
Übersicht 535

älteren Individuen mit möglicherweise kürzlich erworbener To-


xoplasmose und bei lateinamerikanischer Herkunft. Bei nicht op-
timaler diagnostischer Sensitivität und begrenzten therapeuti-
schen Möglichkeiten sollte sich die diagnostische und therapeu-
tische Strategie an der individuellen Situation orientieren.

Introduction The disease was bilateral in 4% of the eyes with acquired OT and
! in 44% of those with congenital OT (p < 0.0001). Differences in the
Ocular Toxoplasmosis (OT) is the main cause of infectious poste- functional consequences of the two sources of infection were also
rior uveitis in most geographical regions of the world (l" Table 1) observed. With a visual acuity of 1.0 (± 1 line) in the better and
[1, 2]. Although the seroprevalence of anti-Toxoplasma antibodies 0.4 (± 5 lines) in the worse eye, better outcomes were observed
in the USA and Europe is on the decline, infection with Toxoplas- in the patients with acquired OT than in those with congenital
ma gondii is still a health hazard of economic dimensions [3, 4]. OT [0.8 (± 4 lines) in the better and 0.25 (± 7 lines) in the worse
An estimated 30% of the world population harbour anti-Toxo- eye (p < 0.05)] [12].
plasma antibodies, with a two-fold higher prevalence in South The burden of the disease in general and of the ocular affection in
America than in either the USA or Europe. In the latter countries, particular is more severe in patients with acquired OT than in
the prevalence of the disease declined by 50 % between the obser- those with congenital OT. The genotype of the parasite contrib-
vation periods from 1988 to 1994 and 2009 to 2010 [3]. Over and utes to the clinical presentation of OT in a relevant degree, and is
above clinically-confirmed cases of infection, the prevalence of linked to the geographic origin of its acquisition (l " Fig. 1) [8]. In-

OT has been estimated to be 2%. Hence, in Europe, approximately dividuals who have been infected in Brazil and Columbia typi-
three million persons carry an active form of the disease and/or cally harbour genotypes I and III, as well as atypical strains,

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harbour infection-associated scars. In 70 % of these cases, asymp- whereas in the vast majority of European cases, the genotype II
tomatic and undetected scars are presumed to exist. However, is resident. The seroprevalence of the infection is 30 % to 50 % low-
robust data in support of this contention do not exist. After infec- er in European than in South American women. This circum-
tion, the prevalence and incidence of ocular symptoms depend stance accounts for the difference in the prevalence and the se-
upon socio-economic factors and the parasitic genotype. Evolu- verity of congenital OT between the two ethnographic groups:
tionarily, the parasite has adopted itself admirably to its host, 3.3/10 000 births in the former and 40/10 000 births in the latter
and today, virtually all mammals and birds are implicated. With- (l" Table 2) [13–15]. Differences in the clinical course of congeni-

in the eye, the parasite contrives to manipulate the immune re- tal OT are also observed between South-American (Brazilian) and
sponse in such a way as to favour its survival without causing European patients: a 5-fold higher incidence of retinochoroiditis
too much damage to the organ [5–8]. As the name implies, toxo- during the first year of life is observed in the former than in the
plasmic retinochoroiditis affects primarily the inner layers of the latter [hazard ratio: 5.4 (3.2–9.1), p < 0.01], a higher recurrence
retina, where the parasites remain dormant within tissue cysts rate (80% versus 34 %, p < 0.01), and a higher incidence of cases
until the flaring up of a recurrence [9, 10]. Consequently, the pri- with a visual acuity below 0.5 (87% versus 29 %, p < 0.0001) [16,
mary site of tissue damage in the case of a recurrence is the reti- 17]. Whilst patients originating from South America frequently
nal nerve-fibre layer, which accounts for the functional impact of manifest severe vision loss, European ones suffer from relevant
the disease. visual-field impairments (l " Fig. 2) [18]. This finding confirms

the general impression that, in the majority of European cases, a


good visual acuity can be sustained in both eyes, irrespective of
Burden of the Disease whether the disease is unilateral or bilateral [19]. Nevertheless,
! each recurrence of OT exposes the patient to the risk of perma-
Acquired infection probably leads more frequently to a clinically- nent functional eye damage [20–24].
symptomatic disease state than does the congenital condition,
with an estimated incidence of 30% of all OT cases. It is mani-
fested in elderly and in immunocompromised individuals,
presents in atypical clinical forms and pursues a comparatively
Table 1 Relevant parameters relating to ocular toxoplasmosis and their inci-
more aggressive clinical course. Hence, from a global health per- dences.
spective, preventive measures are desirable, with a view not only
to preventing a horizontal transmission of the disease from a Incidence
pregnant woman to her child, but also to benefiting the general Prevalence of ocular toxoplasmosis amongst 8.4 %
population [5, 7, 11]. Two-thirds of the patients who consult an individuals with uveitis
ophthalmologist for visual disturbances harbour active lesions, Risk factors: Youth, male gender, Latin origin
Active disease 68 %
whereas one-third of the individuals manifest pre-existing but
Recent (IgM- positive) 12%
hitherto undetected and inactive lesions, which have led to mac-
Unilateral 98%
ular scaring and correspondingly low vision and eventually to as- Pre-existing retinal scars 57%
sociated squinting [1, 2]. In one study that was conducted a few Atypical course 7%
years ago in France, acquired OT was diagnosed in 100 patients Vision loss due to inflammation 74%
of the 425 patients (23%), and congenital OT in 62 patients Macular lesioning 24%
(15%). In the remaining 62% (263 patients), the source of infec- Inactive disease 32 %
tion could not be identified. Patients with acquired OT were sig- Macular scaring 68%
nificantly older (21.7 ± 12.6 versus 9.1 ± 8.8 years, p < 0.0001). Amblyopia 11%

Garweg JG. Ocular Toxoplasmosis: an … Klin Monatsbl Augenheilkd 2016; 233: 534–539
536 Übersicht

Fig. 1 Burden of ocular and neurological disease in


congenital toxoplasmosis of children under six years
of age with various ethnogeographic backgrounds.

Europe [13] Brazil [14] Columbia [15] Table 2 Congenital toxoplasmo-


Parasitic genotype(s) II I, III, atypical I, III, atypical sis in Europe and Southern Ameri-

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Seroprevalence in child-bearing age 1960: 80% 50–80% 50 % ca.
2010: 34%
Risk of infection during pregnancy presumably low High (< 80%) 20 %
Prevalence 3.3/10 000 5–23/10 000 40/10 000
Symptomatic at birth 10–18% 80% 48 %
Macula involvement at birth 2% 21% 50 %
Bilateral involvement 0.7 % 64% 36 %
Neurological signs 5–8% 35%

Fig. 2 Functional consequences of ocular toxo-


plasmosis. An impairment of the visual field is much
more common than a reduction in visual acuity
(94.2 % versus 40.5 %) in European individuals.

Ocular Toxoplasmosis and Recurrences Clinical Diagnostics


! !
In European and North-American cases of OT, recurrence rates of Clinically, it may sometimes be difficult to exclude the onset of
between 54 % and 63 % after each active disease episode have neo-activity in a toxoplasmic lesion. Moreover, new but less ac-
been reported, whereas in South-American ones, values of up to tive lesions outside the fovea may present with unspectacular
80 % have been documented [24–27]. This divergence cannot be symptoms, such as floaters. Hence, if an eye is not examined
accounted for by differences in therapy [28, 29]. Younger patients under red-free illumination conditions, discrete lesions can be
with OT carry a higher risk of developing a recurrence than do easily overlooked. OCT may be helpful in defining disease activity
older ones. After each episode, 55 % to 60% of all OT patients are if the lesion is so placed as to be recorded by this means. If so, dis-
destined to experience another one. The impending risk of a re- ruption, thickening and hyper-reflectivity of the neurosensorial
currence remains a major concern of the affected patients [24, retina are revealed as the early signs of disease activity (repre-
30]. senting the retinal infiltration), followed by disruption of the
photoreceptor layer, changes in the retinal pigment epithelium

Garweg JG. Ocular Toxoplasmosis: an … Klin Monatsbl Augenheilkd 2016; 233: 534–539
Übersicht 537

Fig. 3 Progressive disturbances in vision without a reduction in visual acui- combined manifestations of infiltrations into the retina, focal detachment of
ty. a Image of a primary not highly active ocular lesion in a healthy, 23-year- the vitreous and moderate condensation of the posterior hyaloid. Hyper-
old male patient with an acquired (IgM-positive) form of ocular toxoplasmo- reflective spots are observed also in the pre-retinal vitreous and represent
sis. b OCT-recording in the same patient, revealing hyper-reflective changes leucocytic infiltrations. As yet, the inflammatory changes barely extend into
in the neuroretina around the clinically-visible lesion. The bright spots are the the choroid, Bruchʼs membrane may still be intact.

and thickening of the choroid. The hyper-reflective spots that are (160 mg), administered twice daily for 6 weeks which is generally

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observed pre-retinally resemble the leucocytic infiltration of the well tolerated. This strategy is equivalent to the standard daily
pre-retinal vitreous, which is not infrequently detached at the treatment with Pyrimethamine (50 mg) in combination with Sul-
sites of the active lesions (l " Fig. 3). In the centre of a scared le- fadiazone (1000 mg) 4-times a day and of folinic acid (15 mg)
sion, the atrophic retina usually manifests marked thinning and twice weekly (to prevent anaemia) for 6 weeks. If the hemogram
a loss of its characteristic stratification; the choroid is completely after one week indicates reduced erythro- or leucocyte counts, a
atrophic. In contrast, the margins of the lesion are well de- reduction of the Pyrimethamine dosing to 25 mg daily has to be
lineated, and no vitreal infiltrates are detectable [31–34]. The considered. A frequent therapeutic mistake is to replace folinic
clinical diagnosis needs not as a rule be confirmed in the labora- acid with folic acid, which is considerably cheaper. Since folic acid
tory. However, anti-Toxoplasma antibodies (IgM and IgG) should counteracts the effects of the folic-acid antagonist pyrimeth-
be determined on the onset of a first episode. In atypical cases, a amine (Daraprim®), it neutralizes its anti-parasitic effect. The
confirmation of the diagnosis should be attempted with a view to safety profile of the former therapy is favourable, and the toler-
the therapeutic consequences. A serological analysis may be ance level much higher than that for the latter approach [39, 41,
helpful only in recently-acquired cases. In all unclear and atypical 42]. Intravitreal treatment with a combination of Clindamycin
ones, a combined analysis of the aqueous humour and the serum and Dexamethasone has proved to be as effective as a systemic
for the levels of anti-Toxoplasma antibodies and the presence of therapeutic approach with respect to the ocular outcome [43].
parasitic DNA are advisable to confirm the diagnosis [35, 36]. Us- However, it should be borne in mind, that toxoplasmosis is a sys-
ing this combined approach, a diagnostic sensitivity of 60% to temic affection with local clinical manifestations. Toxoplasmic
70 % is achieved on the basis of a diagnostic specificity of 90 % DNA is regularly detected in the blood, even in the absence of an
[37]. It is pertinent here to mention that sampling for laboratory active ocular disease [6, 44, 45]. Hence, an intravitreal therapeutic
testing should be ideally performed before the onset of treat- intervention does not prevent the occurrence of manifestations
ment, even though falsely-negative results can be registered in in the partner eye. However, there exists evidence that intermit-
cases in which the disease activity is of less than 2-weeks dura- tent prophylactic treatment with Trimethoprim/Sulfamethoxa-
tion [36]. Notably, however, namely in atypical cases with aggres- zole prevents a recurrence of the disease, albeit only for the dura-
sive disease, treatment should be initiated at first presentation tion of the treatment [29, 46, 47]. The question, as to whether a
without delay until receipt of laboratory confirmation. Depend- prophylaxis of recurrences is needed in the context of intraocular
ing on the choice of therapeutic strategy, laboratory testing surgery is still a matter of debate. However, existing evidence is
should also be undertaken during the course of treatment to ex- not strongly supportive of its necessity [48].
clude a toxic working of the anti-parasitic drugs [28, 39, 40]. In the end, the most critical question is, in which situation is a po-
tentially toxic treatment justified. In the absence of evidence to
the contrary, specialists are of the consensus that patients with
Therapy and Prophylaxis of Ocular Toxoplasmosis central lesions and frequent recurrences warrant treatment. If
! there is a strong inflammatory response, combined treatment
The treatment and prophylaxis of active OT have been widely dis- with antibiotics and steroids may be an option to hasten a resolu-
cussed [29, 36]. There exists conflicting evidence as to the effec- tion of the visual complaints. Treatment is called for in South-
tiveness of systemic or intravitreal treatment with antibiotics in American individuals, owing to the more severe clinical courses;
European cases of toxoplasmic retinochoroiditis. No antibiotic likewise in immunocompromised patients and in those under-
regimen has distinguished itself as being superior to any other going iatrogenic immunosuppression. The available therapeutic
[28]. One currently used approach (except in individuals who options should be discussed with the patient if only one eye is im-
are allergic to sulphonamides) involves systemic treatment with plicated. No therapy is justified for small lesions lying in the pe-
a combination of Trimethoprim (800 mg) and Sulfamethoxazole riphery of the retina, external to the vascular arcades and one-

Garweg JG. Ocular Toxoplasmosis: an … Klin Monatsbl Augenheilkd 2016; 233: 534–539
538 Übersicht

disc-diameter away from the optic- nerve head. Clearly, steroids 18 Scherrer J, Iliev ME, Halberstadt M et al. Visual function in human ocular
toxoplasmosis. Br J Ophthalmol 2007; 91: 233–236
should not be administered without antibiotic coverage [28, 39].
19 Wallon M, Garweg JG, Abrahamowicz M et al. Ophthalmic outcomes of
The combined antibiotic and steroid approach should be confined congenital toxoplasmosis followed until adolescence. Pediatrics 2014;
to patients with an exaggerated inflammatory response, since it 133: e601-e608
remains unclear, whether supplementary treatment with cortico- 20 Friedmann CT, Knox DL. Variations in recurrent active toxoplasmic ret-
steroids does indeed effect an improvement in the outcome over inochoroiditis. Arch Ophthalmol 1969; 81: 481–493
21 Gilbert RE, Dunn DT, Lightman S et al. Incidence of symptomatic toxo-
and above that achieved with anti-parasitic agents alone [49].
plasma eye disease: aetiology and public health implications. Epide-
In conclusion, it is important to consider OT in the differential di- miol Infect 1999; 123: 283–289
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genital and acquired forms of the disease cannot be made on the gondii infection in southern Brazil. Am J Ophthalmol 2001; 131: 351–
basis of clinical presentation and course. Younger patients carry a 354
23 Bosch-Driessen LE, Berendschot TT, Ongkosuwito JV et al. Ocular toxo-
higher risk of experiencing recurrences than do older ones, and
plasmosis: clinical features and prognosis of 154 patients. Ophthal-
they are more likely to manifest a connatally-attracted form of mology 2002; 109: 869–878
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eradicating the infection. After each episode, 55% to 60 % of all pa- European patients with ocular toxoplasmosis. Br J Ophthalmol 2008;
92: 1253–1256
tients will develop a recurrence [24, 36].
25 de-la-Torre A, Rios-Cadavid AC, Cardozo-García CM et al. Frequency and
factors associated with recurrences of ocular toxoplasmosis in a refer-
ral centre in Colombia. Br J Ophthalmol 2009; 93: 1001–1004
Conflict of Interest 26 Holland GN, Crespi CM, ten Dam-van Loon N et al. Analysis of recurrence
! patterns associated with toxoplasmic retinochoroiditis. Am J Ophthal-
mol 2008; 145: 1007–1013
The author has no conflicting financial interests in this manu-
27 Reich M, Ruppenstein M, Becker MD et al. Risk of Recurrence of Preexist-
script. ing Ocular Toxoplasmosis during Pregnancy. Ocul Immunol Inflamm

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Garweg JG. Ocular Toxoplasmosis: an … Klin Monatsbl Augenheilkd 2016; 233: 534–539