Seroprevalence and molecular epidemiology of Toxoplasma gondii in the Western Cape of South Africa

Hammond-Aryee, Kenneth Nii Ofei (2016-12)

Thesis (PhD)--Stellenbosch University, 2016.

Thesis

ENGLISH SUMMARY: Toxoplasmosis is a disease caused by the obligate intracellular parasite Toxoplasma gondii and is one of the most widely occurring infections known to man, causing disease in almost all mammals and warm-blooded birds. Toxoplasma gondii is an opportunistic pathogen, taking advantage of weakened immune systems to cause disease. The disease toxoplasmosis is known to occur in both active and latent or chronic forms. The latent or chronic form of toxoplasmosis is known to be the most common latent infection in man. Currently, the effects of the latent or chronic form of toxoplasmosis is neither properly studied nor understood. In Africa, there is currently no systematic monitoring or reporting of toxoplasmosis incidence or T. gondii prevalence and this leaves health systems at a disadvantage. The United States Centre for disease Control and Prevention (CDC) currently classify toxoplasmosis as a neglected tropical infection. In this series of research projects, the seroprevalence of T. gondii antibodies and the risk factors to infection were investigated. Following that, the molecular epidemiology and population structure of the pathogen was also investigated. The investigations were conducted in opportunistically selected human and animal populations within the Western Cape Province of South Africa. The data obtained was analyzed from a “One World One Health” perspective and conclusions were then documented. The selected human populations were, a cohort of human immunodeficiency virus (HIV) positive and human immunodeficiency virus (HIV) negative post parturient women and their HIV exposed and uninfected (HEU) and HIV unexposed and uninfected (HUU) infants, and a cohort of HIV positive and HIV negative male and female patients presenting with a clinical diagnosis of uveitis at the Tygerberg academic hospital opthalmology clinic. The selected animal populations were a population of feral cats in the greater Cape Town metropole, a population of free ranging sheep on a single farm in Bredasdorp and a population of free ranging caracals in the Cape peninsula region. Toxoplasma gondii seroprevalence was 23.3% in the cohort of post parturient women, whilst the seroprevalence in the infant cohort was 1.02%. The seroprevalence was 24.7% in the cohort of patients presenting with ocular infections. The seroprevalence was not associated with HIV status but was associated with the consumption of unwashed fruits and vegetables. The similarity between the seroprevalence in the post parturient cohort and the ocular cohort points to the lack of regional differences in seroprevalence rates, whilst the low seroprevalence in the infant cohort implies a low rate of congenital toxoplasmosis in the study area and this comforms to what is observed in other parts of Africa, Europe and North America. Seroprevalence was extremely high in the felid populations investigated (Feral cats - 37.1% and Caracals- 69.6%). These justifies considerable attention since these felids were free ranging and therefore have access to domestic human and animal populations. The seroprevalence in the sheep flock was also higher at 8.0% than the five point six percent (5.6%) reported in earlier studies in Cape Town. Current research has established that T. gondii genotypes vary in their geographic distribution, with certain genotypes being more predominant in certain geographic areas than others. To establish the genotypes of T. gondii present in our selected geographic area, we investigated the molecular epidemiology of the pathogen. The molecular epidemiology investigations revealed a predominance of Type II genotypes in both human and animal samples. A Type III genotype was detected in human but not in animal samples. Atypical genotypes were also identified in both human and animal samples. The observed population structure is similar to that of South America and other parts of Africa but differs from that observed in Europe and North America. We have demonstrated the presence of T. gondii as well as its active transmission within selected human and animal populations in the Cape Town metropole of South Africa. The presence of atypical T. gondii genotypes was also demonstrated. The observed seroprevalence rates investigated in this study implies that more attention needs to be paid to the disease as it could have implications for female reproductive health, infant to adolescent ocular health as well as overall economic losses due to an increase in disease burden in humans (reported as disability-adjusted life years) and for agriculture.

AFRIKAANSE OPSOMMING: Toksoplasmose is 'n siektetoestand wat veroorsaak word deur die intrasellulêre-gebonde parasiet Toxoplasma gondii is 'n opportunistiese patogeen, wat voordeel trek uit verswakte immuunstelsels om die siekte te veroorsaak Toksoplasmose is een van die mees wyd verspreide infeksies wat bekend is aan die mens, en affekteer baie, indien nie die meeste, soogdierspesies en voëls. Toksoplasmose kom voor in beide aktiewe en latente vorms, en dit is bekend dat die latente vorm van toksoplasmose die mees algemene latente infeksie in die mens is, en die gevolge daarvan is nog nie behoorlik bestudeer of word verstaan nie. In Afrika, is daar tans geen sistematiese monitering of verslagdoening oor die voorkoms van toksoplasmose óf Toxoplasma gondii nie en dit benadeel tans gesondheidbestuur. Die “Centre for Disease Control (CDC)” in die Verenigde State van Amerika klassifiseer toksoplasmose tans as 'n afgeskeepte tropiese infeksiesiekte. In hierdie reeks navorsingsprojekte word die serologiese voorkoms van T. gondii teenliggame en die risikofaktore wat tot infeksie lei, ondersoek. Hierop volg dan ‘n verdere ondersoek na die molekulêre epidemiologie en populasiestrukture van die patogeen. Die navorsing is uitgevoer op opportunisties geselekteerde mens- en dierbevolkings binne Suid-Afrika. Die data wat verkry is, is verwerk vanuit ‘n “One World One Health” perspektief en gevolgtrekkings is hiervolgens gemaak. Die geselekteerde menslike bevolking het bestaan uit 'n groep MIV-positiewe en MIVnegatiewe na-swangerskap vroue-pasiënte met hul MIV-blootgestelde en onbesmette (HEU), en MIV-onblootgestelde en onbesmette (HUU) kinders, asook 'n groep van manlike en vroulike pasiënte met okulêre infeksies gediagnoseer by die Tygerberg Hospitaal oogkliniek. Die geselekteerde dierebevolkings het bestaan uit 'n bevolking van wilde katte in die groter Kaapse metropool, 'n bevolking van vry weiende skape op n enkele plaas, en 'n bevolking van los-lopende rooikatte in die Kaapse skiereiland, almal in die bestek van die Wes-Kaap Provinsie van Suid-Afrika. Seroprevalensie van T. gondii was 23.3% in die groep van na-geboorte vroue terwyl prevalensie 1.02% in die kindergroep was. Die seroprevalensie was ook hoog, teen 24.7%, in die groep van pasiënte met okulêre infeksies. Die seroprevalensie was nie verbind met MIV-status nie, maar wel met die verbruik van ongewaste vrugte en groente. Die ooreenstemming in die seroprevalensie van die na-geboorte groep en die ooginfeksie groep dui op ‘n area-verskil in seroprevalensie tempo, terwyl die lae seroprevalensie in die kinder-groep dui op ‘n lae tempo van aangebore toksoplasmose in die area van studie en dit stem ooreen met waarnemings in ander dele van Afrika, Europa en Noord- Amerika. Seroprevalensie was baie hoog in die wilde kat bevolkings (wildekatte –37.1% en in Rooikatte- 69,6%). Hierdie bevinding vereis verdere aandag omdat die katte vrylopend was en daarom toegang gehad het tot die plaaslike mens- en huisdierbevolkings. Die seroprevalensie in die skaapbevolking was ook hoër teen 8.0% teenoor die 5.6% wat in vorige studies gerapporteer was in Kaapstad. Huidige navorsing het bepaal dat T.gondii genotipies varieër in hul geografiese verspreiding, met sekere genotipes meer dominant in sekere geografiese area’s as ander. Om die genotipes van T.gondii in ons geselekteerde geografiese gebied te bestudeer , het ons die molekulêre epidemiologie van die patogeen bepaal. Die molekulêre epidemiologiese ondersoeke het aangedui op 'n oorheersing van Tipe II genotipes in beide mens- en dier monsters. Tipe III genotipes was gevind in die menslike siektevorm, maar nie in die dier-infeksie monsters nie. Atipiese genotipes is ook waargeneem in beide mens- en dieremonsters. Die waargeneemde bevolkingstruktuur van Toxoplasma gondii is soortgelyk aan dié van Suid-Amerika en ander dele van Afrika, maar verskil van dié wat waargeneem word in Europa en Noord-Amerika. Ons het die teenwoordigheid van T. gondii asook sy aktiewe oordrag binne die geselekteerde mens en dier bevolkings in die Wes-Kaap van Suid-Afrika bewys. Die teenwoordigheid van atipiese T.gondii genotipes word ook beskryf. Die waargeneemde seroprevalensies wat in hierdie studie ondersoek is, dui daarop dat meer aandag gegee moet word aan die siekte, omdat dit ernstige implikasies inhou vir vroulike reproduktiewe gesondheid, baba tot adolessent okulêre gesondheid, asook ‘n hoë lading op die gesondheidstelsel en in die landbou plaas as gevolg van 'n toename in siektelas in die mens.

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