Ocular Immunology and Inflammation

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Ocular Toxoplasmosis in Africa: A Narrative Review

of the Literature

Nadine Nsiangani-Lusambo , Juliana Reyes-Guanes , Pilar Uribe-Reina ,

Dieudonné Kaimbo Wa Kaimbo , Dieudonné Mumba Ngoyi & Alejandra de-
la-Torre

To cite this article: Nadine Nsiangani-Lusambo , Juliana Reyes-Guanes , Pilar Uribe-Reina ,

Dieudonné Kaimbo Wa Kaimbo , Dieudonné Mumba Ngoyi & Alejandra de-la-Torre (2020):
Ocular Toxoplasmosis in Africa: A Narrative Review of the Literature, Ocular Immunology and
Inflammation, DOI: 10.1080/09273948.2020.1801761

To link to this article: https://doi.org/10.1080/09273948.2020.1801761

Published online: 25 Sep 2020.

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OCULAR IMMUNOLOGY AND INFLAMMATION
https://doi.org/10.1080/09273948.2020.1801761

INVITED REVIEW

Ocular Toxoplasmosis in Africa: A Narrative Review of the Literature

Nadine Nsiangani-Lusambo MDa, Juliana Reyes-Guanes MD b,c, Pilar Uribe-Reina MD b,c,
Dieudonné Kaimbo Wa Kaimbo MD PhDa, Dieudonné Mumba Ngoyi MD PhDd, and Alejandra de-la-Torre MD PhD c

a
Eye Department, University Clinic, Medical School, University of Kinshasa, Kinshasa, Democratic Republic of Congo; bEscuela Superior de Oftalmología
del Instituto Barraquer de América, Bogotá, Colombia; cGrupo de Investigación en Neurociencia (Neuros), Escuela de Medicina y Ciencias de La Salud,
Universidad Del Rosario, Bogotá, Colombia; dParasitology Department, University Clinic, Medical School, University of Kinshasa, Kinshasa, Democratic
Republic of Congo

ABSTRACT ARTICLE HISTORY

Purpose: To present a narrative review about ocular toxoplasmosis epidemiology, disease burden and Received 31 May 2020
prevalent African parasitic strains. Revised 6 July 2020
Methods: An initial search for MeSH terms was conducted with a posterior advanced search in two Accepted 23 July 2020
electronic databases. Full text reading was performed. KEYWORDS
Results: Animal African studies have identified Toxoplasma gondii type II, type III, Africa 1, and Africa 3 Africa; Toxoplasma; ocular
strains. Seroprevalence varies from 6.4% to 74.5%. Nevertheless, there is a scarcity of epidemiology and Toxoplasmosis;
serotyping information about ocular toxoplasmosis. African studies have demonstrated that uveitis epidemiology; risk Factors
patients present high frequencies of ocular toxoplasmosis. There is a lack of studies describing specific
clinical characteristics, which can be related, to environmental and socioeconomic factors, parasite
serotype and genotype, and genetic susceptibility of the host.
Conclusion: As Toxoplasma gondii has more virulent strains in the Southern hemisphere, it is relevant to
determine African strain types and the correlation between the infecting strains and the clinical
manifestations.

Toxoplasma gondii (Tg), an obligate intracellular parasite,1 is the present a narrative review about OT epidemiology, the burden
most common cause of posterior uveitis and focal retinitis.2 It of disease and the most prevalent strains in Africa.
causes permanent visual impairment in more than 25% of patients
and can lead to legal blindness.3,4 The seroprevalence of Tg varies
Materials and methods
from country to country and even by regions. These differences
could be related to environmental and socio-economic factors.3,5 An initial search was performed in the PubMed database for
Tg infects around one-third of the world´s population. The articles of relevance in the subject to be discussed to filter the
parasite strains have a geographical distribution with MeSH terms and key words. These were used separately or in
a predominance of biphasic pattern consisting of regions in combination to perform an advanced search in two electronic
the Northern Hemisphere where a few, highly clonal and databases in the following manner: PubMed, (ocular toxoplas­
abundant lineages predominate (less virulent); elsewhere, and mosis [MeSH Terms]) AND africa[MeSH Terms]), and
especially in portions of South America are characterized by LILACS: (toxoplasmosis [Categoria DeCS] and africa
a diverse assemblage of less common genotypes that show [Categoria DeCS]). Relevant articles up to April 2020 were
greater evidence of recombination (more virulent).4 South recovered, without any publication year limit. Subsequently,
America, as the continent with the most virulent strains, has we read the full text of all the articles and obtained the infor­
more epidemiological data. Ocular toxoplasmosis (OT) preva­ mation and new bibliographies necessary to address the topics
lence reaches up to approximately 18% in this continent. of interest in the present narrative review.
Countries such as Colombia and Brazil present prevalence of
about 6% and 17.7%, respectively, and patients present more Worldwide background
severe ocular compromise. On the other hand, North America
and Europe present a prevalence of 2% and a less severe Epidemiology of Tg Infection Worldwide
disease. Few ocular toxoplasmosis studies have been developed Seroprevalence
in Asia, as it has less virulent strains, and no consensus about Although Tg infects around one-third of the world’s
prevalence has been reached. In the same way, there are no data population,10 and it is a major public health concern in many
about the prevalence of OT in Australia in the general countries, seroprevalence of this parasite differs greatly around
population.6–9 Similarly, Africa remains understudied regard­ the world. It presents rates from 10 to 30% in Asia, North
ing the prevalence of OT.10,11 The aim of this article is to America and North Europe. In India prevalence has reported

CONTACT Alejandra de-la-Torre [email protected] Research Group in Neurosciences NeURos. Escuela de Medicina y Ciencias de La Salud, Universidad
del Rosario, Bogotá, Colombia
© 2020 Taylor & Francis Group, LLC
2 N. NSIANGANI-LUSAMBO ET AL.

Figure 1. Worldwide distribution of Tg strains and OT geographical distribution.

to be 24.8%.12 and 125% in China.13 In the United States it has In Ethiopia, a series of studies carried out on domestic
dropped though years to 9%.14 In Norway pregnant women animals (sheep, goats, camels, chickens, and pigs) revealed
prevalence has shown to be 10.9%. On the other hand, in a high seroprevalence, varying between 17.7% and 49.6%
Central and Southern Europe, values go from 30 to 50%; as the depending on the species.36–40 Three strains of Tg were isolated
latitude decreases, the prevalence increases.6 Finally, it presents from sheep and goats’ samples: Type II (the most frequent),
very high rates in South America and tropical Africa.5,15 Several Type III, and atypical strains.41 Samples from the East Shewa
articles have discussed Brazil prevalence, ranging from 29.3%16 province showed higher genetic diversity, it could be explained
to 80.4%,17 depending on the geographical region. In Colombia by the diverse agro-ecologies in this area (altitude ranging from
seroprevalence goes up to 47%.18 These differences are related to 953 to 3400 masl).37
environmental factors such as climate and presence of the defi­
nitive host, and socio-economic factors such as hygienic condi­ Human Tg Infection in Africa
tions and eating habits.5 In Africa, human seroprevalence of Tg infection varies from 6.4
to 74.5%, depending on the country, with a median of 35%.24
Types of Tg Strains and OT Geographical Distribution A study about seroprevalence of toxoplasmosis in pregnant
Worldwide distribution of Tg strains and OT geographical women conducted in Africa and Arabia revealed a higher pre­
distribution are shown in Figure 1 4,8,19-21 valence in Central Africa, especially in Democratic Republic of
Congo (DRC).42 In Democratic Republic of São Tomé and
Epidemiology of OT around the World until Now Príncipe (DRSTP), West Africa, the overall seroprevalence of
Below, in Table 1, we present clinical and immunological Tg infection among primary schoolchildren was 63.1%.43 The
consequences of Tg strain diversity in human OT worldwide. Tg antibodies seroprevalence was also high among pregnant
women in Southwestern Ethiopia (81.1%),44 as well as in
Tanzania (30.9%).45 A population-based study carried out in
Africa background Ghana, in 3 districts of the country found a seroprevalence of
Tg infection around 85%.46 Another study, performed among
Epidemiology of OT in Africa up to Now
pregnant women in Accra, noted a seroprevalence of 92.5%.41
Animal Tg Infection in Africa In Central Africa, Toxoplasmosis is highly prevalent in
In Africa, there is a lack of information about Tg strains in the Kinshasa, the capital of DRC. A study conducted among preg­
continent. In Algeria, a study conducted on rats identified type nant women found a seroprevalence of 80.3%, higher than the
II as the most prevalent Tg strain in the country.34 Meanwhile, African average.38 One woman out of 25 had a recent toxoplas­
a study on animals in Gabon presented type III as the most mosis infection and 20% were not protected against primo-
common serotype. In addition, two new parasite serotypes infection, indicating a need for measures to prevent and control
where identified; Africa 1 and Africa 3, the first one being toxoplasmosis during pregnancy.47
more virulent. These Africa 3 strain could be linked to those Here, in Table 2, we present a summary of Tg serotyping
found in Central and South America.35 studies in Africa. Nevertheless, most of these studies have been
 OCULAR IMMUNOLOGY AND INFLAMMATION 3

Table 1. Consequences of strain diversity.

Clinical Consequences ● Responsible of 85% of posterior uveitis in immunocompetent patients.22
● In Europe and United States, toxoplasmosis was found as etiology of uveitis in 4–8% of patients.5,23
● OT causes permanent visual impairment in more than 25% of patients.8,24
● Clinical consequences in congenital and acquired OT are different in Europe, compared to South America.25,26
● South American patients, infected often by virulent strains (type I, III and atypical), have more severe OT, larger lesions, more
inflammation, and a Th2 deviated immune response.26,27
● European patients, infected regularly by less virulent strains (mostly type II), present mild OT, less inflammation, smaller lesions, and
a Th1/Th17 deviated immune response.26–28
● A study in a large cohort of neonates in Brazil demonstrated 80% had retinal involvement and 50% active lesions. This suggested
a more severe ocular involvement in Brazil than other parts of the world.29
● Rhoptry protein (ROP) 16 and ROP18 virulent factors are important in human OT. The absence of Toxoplasma ROP18 promoter insertion
sequence in OT was correlated with severe ocular inflammatory response in Colombian patients.30 It was also found that the majority of
ROP16 nucleotide sequences from Colombian patients with OT belonged to the group of mouse-virulent strains.31
Immunological ● South American patients, infected with more virulent strains, presented decreased IFN-ɤ and IL-17 and increased IL-6 and IL-13
consequences intraocular levels. These results are consistent with the hypothesis that South American strains could be responsible for a greater OT
severity, by inhibiting the IFN-ɤ protective factor, and deviating immune response to Th2.28
● Deviated immune response can be observed locally, as an intraocular response32 or systemically.33
● Genetic susceptibility of the host could also be involved; polymorphism of genes encoding host cytokines could have some influence.5,6

Table 2. Toxoplasma serotyping and genotyping studies in Africa.

Author Year Country Subjects Sample Serotype
Dubey48 2004 Egypt Chicken 20 Type III 85% Type II 15%
Dubey49 2005 Democratic Republic of Congo Chicken 10 Type III 80% Type II 10% Type I 10%
(DRC)
Sousa50 2008 East and Central Africa Immunocompetent and 89 Type I/III 31.5% Type II 11.2%
immunocompromised patients
Velmurugan51 2008 DRC, Egypt, Nigeria, Kenya, Chicken 19 Type III 68.4% Type II 26.3% Atypical 5.3%
Burkina Faso
Lindstrom52 2008 Uganda Chicken 20 Type III 40% Type I 30% Type II 5% Multiple 25%
Mercier35 2010 Gabon Animals 425 Type III Africa 1 and 3
Boughattas53 2010 Tunisia Cases of congenital toxoplasmosis 14 Type I 7.1% Type I/III 50% Type I/II 21.4% Type I/III
+I/II 21.4%
Ndiaye54 2013 Senegal Animals 10 Africa 1 90% Africa 2 10%

developed in animals. Thus, there is a scarcity of information (DRC) (2019) and another in Egypt (2019) found OT as the
in toxoplasmosis serotyping in African population and there is principal cause of posterior uveitis.63,64 In a 3-year retrospective
no information about OT serotyping. study carried out in DRC, toxoplasmosis was found to be the
most common etiology of uveitis, with a prevalence of 25.1%.
Prevalence of OT From the patients with OT, 74.3% had chorioretinal lesions that
Toxoplasmosis in known to be a preventable cause of blind­ involved the central retina.63
ness. An adequate knowledge of its characteristics may help to In Sierra Leone, West Africa, uveitis was associated with
improve its management.8 Despite the high seroprevalence, severe visual impairment in patients with infectious diseases.
mentioned above, there are not enough studies on OT in Toxoplasmosis proved to be the most important cause of
Africa. uveitis, with a prevalence of 43%. Although the distribution
Besides the high seroprevalence, there is a high frequency of of congenital versus acquired toxoplasmosis could not be
ocular manifestations of the pathology. An English study estab­ determined, the results indicate an important role of postna­
lished that the incidence of ocular symptoms in patients with tally acquired disease. The study further suggested minor roles
retinochoroidal lesions due to toxoplasmosis was 100 times for HIV, tuberculosis, toxocariasis, and sarcoidosis as causes of
more common among African-born patients compared to uveitis.56 Similarly, a population-based study carried out in
other groups.55 Ghana, found lesions of OT in 2.6% of the cases.46
Studies in Africa have demonstrated that patients with uveitis Although it has been stablished that OT is the most common
present a higher frequency of OT, ranging from 29 to 58%.56–59 cause of uveitis in some places of Africa, there is a scarcity of data
In 1993, a study about chronic uveitis was carried-out at the regarding specific clinical characteristics of intraocular infection
Kinshasa Uveitis Clinic, 6% of the patients presented toxoplas­ in this continent. In Sub-Saharan Africa, three studies on OT, in
mosis as etiology and it was the second cause of posterior Ghana,65 Sierra Leone,56 and DRC,63 found unilateral involve­
uveitis.60 In 2011, another study in the same hospital, this time ment in the majority of patients, ranging from 61.29% to 90.9%.
on HIV-positive patients, presented toxoplasmosis as the etiol­ These studies suggested a predominance of the acquired forms
ogy in 10% of cases and was the second cause of posterior uveitis of the pathology. Chorioretinal lesions were associated with
after cytomegalovirus retinitis.61 Similarly, a study in Cape Town visual impairment in around 70% of the cases.63,65 The Sierra
in 2017, showed syphilis as the most common uveitis infectious Leone study56 established panuveitis as the most common ana­
cause, followed by toxoplasmosis with a prevalence of 8.6%.62 tomic presentation, followed by posterior uveitis, anterior uvei­
Nevertheless, two studies, one in Democratic Republic of Congo tis, and intermediate uveitis. Complications presented by these
4 N. NSIANGANI-LUSAMBO ET AL.

Table 3. Toxoplasma gondii infection risk factors in Africa.

Author Country Year Sample Population Seroprevalence Risk factors
Hung69 São-Tomé 2007 499 Pregnant women 75.2% Age/Pet ownership/Raw meat consumption/
Unwashed vegetables consumption/
Untreated water consumption
Ayi41 Ghana 2009 294 Pregnant women No data Own a cat
Doudou47 Democratic Republic of Congo 2014 781 Pregnant women 80.3% No significant factor found
Kwasi46 Central Region of Ghana 2014 425 Ghana communities 85% Contact with soil/Disposal of cat litter/
Keeping of cats/Source of drinking water
Ohiolei70,71**** Nigeria 2016 Non applicable Review of studies 32% Age between 51–60 years/Professions with
ground or animal contact/Undercooked
meat, Unpasteurized milk and raw
vegetable consumption/Own a cat or
a dog
Savi de Tové51 Benin 2018 399 Pregnant women 36.1% Raw vegetable consumption

patients were: cataracts, glaucoma, vitreous hemorrhage, retinal the parasite factors such as Tg strains and their virulence; as
detachment, blindness, and visual impairment. Contrarily, the well as factors related to the host.
DRC63 study proposed posterior uveitis was the most common In the same way, it is necessary to evaluate the epigenetic
type, followed by panuveitis, associated with posterior pole ret­ influence among OT infection in order to reach prevention, early
inal scars and macular and yuxtapapilar lesions. Additionally, diagnosis, and adequate treatment. This, with the purpose of
the Ghana study65 proposed that size lesions where in their reducing infection rates, recurrences, and disease complications.
majority smaller than 2 disk diameters; but bigger retinal scars
were more likely to cause symptoms and complications.
The appearance of clinical manifestations in OT can be Conclusion
related, as well, to environmental and socioeconomic factors,
OT is one of the most common causes of posterior infectious
parasite serotype and genotype, and genetic susceptibility of the
uveitis in Africa. Although, multiple serotypes and strains have
host. OT lesions are mostly associated with type I and atypical Tg
been described in Africa (Type I, II, III, Africa 1 and 3 and
strains.19 A serotyping study carried out in human samples from
atypical strains), there is no general African consensus about
3 continents (Europe, Africa and South America) was able to
the impact of this disease and the most prevalent strains asso­
identify an association of genes in types I and II in 31.5% of
ciated with ocular involvement.
African patients coming from Eastern and Central African
Considering the fact that Africa is a continent located in the
countries.50 Some authors have noted that the polymorphisms
same geographical hemisphere as South America, and that Tg
of genes encoding host cytokines could have some influence in
has a biphasic geographical distribution (Northern and
the development of OT.5,6 In the same way, a study carried out in
Southern hemisphere with less and more virulent strains,
West Africa highlighted the influence of genetic polymorphisms
respectively), it would be relevant to determine the types of
in the occurrence of OT in Ghanaian population.66
Tg strains implicated in ocular infections in Africa. In addition,
it would be of interest to analyze if there is a correlation
OT Risk Factors between the infecting strains and the clinical manifestations
Some studies have identified risk factors associated with OT, of ocular disease as well as the burden of ocular toxoplasmosis
worldwide. These recognize dietary factors, age, level of educa­ in this geographical region.
tion, and the presence of the definite host as positive risk
factors for Tg infection.67,68
In Africa, factors such as older age, pet ownership, consump­ Acknowledgments
tion of meat, water, and vegetables have been associated with Tg
No acknowledgements to be made.
infection. In a population-based study in Ghana, age and contact
with soil and cats were associated with an increased risk of OT.46
In Table 3 we present a summary of Tg infection seropre­ Authorship
valence and risk factors in Africa.
Other factors, such as type of infection (congenital or All authors attest that they meet the current ICMJE criteria for
acquired), genetic predisposition, and immune status of the Authorship.
host, parasite genotype, load of the inoculum, infection by
oocyst or by tissue cysts, between others, may influence the
Declaration of interest
clinical findings and prognosis of OT. These can have an impact
on severity and risk of recurrence of the infection.8 However, no The authors report no conflicts of interest. The authors alone are respon­
studies in Africa about these topics have been carried out. sible for the content and writing of the paper.

Perspectives
Funding
It is necessary to develop further studies regarding the burden
of OT in the African continent and its possible association with No funding was received to carry out this report.
 OCULAR IMMUNOLOGY AND INFLAMMATION 5

ORCID 19. Xiao J, Yolken RH. Strain hypothesis of Toxoplasma gondii infec­
tion on the outcome of human diseases. Acta Physiol (Oxf). 2015
Juliana Reyes-Guanes MD http://orcid.org/0000-0002-2326-7213 Apr;213(4):828–845. doi:10.1111/apha.12458.
Pilar Uribe-Reina MD http://orcid.org/0000-0001-9088-5903 20. Fuentes I, Rubio JM, Ramírez C, Alvar J. Genotypic characteriza­
Alejandra de-la-Torre MD PhD http://orcid.org/0000-0003-0684-1989 tion of Toxoplasma gondii strains associated with human toxo­
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