Toxoplasma gondii Infections in Southern Africa: History
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Subjects: Parasitology
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Toxoplasma gondii is an apicomplexan parasite with zoonotic importance worldwide especially in pregnant women and immunocompromised people. There is limited information on the distribution of T. gondii in animals and humans in southern African countries. The overall pooled prevalence is estimated as 17%.

  • Toxoplasma gondii
  • infections
  • southern Africa
  • animals
  • humans

1. Introduction

Toxoplasma gondii is an apicomplexan obligate parasite that infects animals and humans worldwide [1]. The definitive hosts are felids although a recent study showed developmental success in mice subjected to certain enzymatic inhibition and diet modification [2]. The intermediate hosts include terrestrial and aquatic mammals and birds [2,3]. The pathways of T. gondii infection and transmission are multifaceted, involving the three developmental stages (tachyzoite, bradyzoite, and sporozoite) of the parasite’s life cycle [2]. Intermediate hosts, including humans, can acquire infection via (i) consumption of water, vegetables, and fruits contaminated with infective oocysts; (ii) consumption of raw or undercooked meat infected with tachyzoites or bradyzoites [4]; (iii) blood transfusion; (iv) organ transplant containing cysts or tachyzoites; and (v) congenital transmission from the mother to fetus via the placenta. Feline definitive hosts acquire infections via the ingestion of sporulated oocysts or by carnivorism. However, rarely, consumption of non-pasteurized milk or milk products can serve as a potential source of T. gondii transmission [2,5,6]. Oysters and mussels can act as reservoir hosts for infective oocysts, which can later be transmitted to other animals upon consumption [2,7,8,9]. Parasites attain maturity in the intestine of felids and start releasing numerous oocysts into the environment within three to 18 days post-infection [10].
Furthermore, Toxoplasma infection in animals or humans causes toxoplasmosis which is prevalent worldwide. The infection rate varies according to geographic region and climatic conditions [1]. Other risk factors of infection include age, gender, farm management, and geographic characteristics [5]. Toxoplasmosis is accompanied by varying degrees of clinical symptoms depending on the inoculum size, virulence of parasite strain, and level of host immunity [11]. Toxoplasma infections have been reported to alter reproductive parameters in hosts by having a negative impact on harming female reproductive functions [12], inducing apoptosis in spermatogonial cells directly or indirectly [13], thereby resulting in reduced quality of human sperm [14] and decreased fertility in experimentally infected male rats [13,15]. A significant association has been reported between T. gondii seropositivity and abortion in small ruminants from certain districts of central Ethiopia [16]. In sheep, an infection may cause early embryonic death and resorption, fetal death and mummification, abortion, and stillbirth, [17] thereby resulting in severe economic loss in the livestock industry [1,3]. The economic impact of T. gondii infection in sheep and other livestock is abortions and increased lambing/kidding interval, culling of infected animals, reduced milk production, and reduced value of the breeding stock, hence leading to major economic losses [16]. The severity of infection is dependent on the stage of gestation the ewe acquires infections. Infection at the early gestational stage often results in fatal consequences [16,18]. In immunocompetent hosts, toxoplasmosis may be asymptomatic, whereas in immunocompromised humans, particularly AIDS patients, the disease has serious consequences [3,19]. Similarly, infection in pregnant women is associated with congenital toxoplasmosis, and the severity and risk are dependent on the time of maternal infection and often accompanied by developmental malformation, abortion, or reduced quality of life for the child [3,11,19].
While toxoplasmosis is a zoonosis that can be controlled or prevented in humans and animals worldwide, in sub-Saharan Africa, the control is hampered by various factors, including high poverty level, lack of diagnostic capacity, limited disease surveillance, and poor veterinary care [20]. Since the fecal-oral route and consumption of raw or undercooked infected food or meat constitute the major transmission route in humans [11], effective control of toxoplasmosis requires adequate awareness of good veterinary practices, personal hygiene, improved culinary habits, dietary habits, and correct diagnosis.
Diagnosis involves direct methods, immunodiagnostic methods, and molecular techniques. The direct method involves isolation of parasite or bioassay, cellular culture, and histology. Immunodiagnostic methods include the Sabin–Feldman dye test (SFT), hemagglutination assay, immunofluorescent assay (IFA), modified agglutination test (MAT), avidity, western blot, enzyme-linked immunosorbent assay (ELISA), recombinant antigens, immunocytochemistry, and immunohistochemistry. Molecular techniques include Polymerase Chain Reaction (PCR), real-time PCR, PCR-restriction fragment length polymorphisms (PCR-RFLP), loop-mediated isothermal amplification (LAMP), and high-resolution melting (HRM) [21].
Toxoplasma gondii infection is accompanied by the emergence of IgM in the host, followed by the appearance of IgA and IgE at about two weeks post-infection [22,23] while IgG spikes around four months post-infection and persists throughout lifetime [23]. Toxoplasmosis in immunocompetent individuals resolves without treatment [24], but in immunocompromised individuals, clindamycin, sulfonamides, spiramycin, and pyrimethamine are used for treatment [25,26]. Pyrimethamine and sulfadiazine drug combination is suitable for new-borns, infants, and pregnant women; however, to prevent transmission from mother to unborn fetus, an antibiotic (spiramycine) has been proven effective but not in latent infections, as antibiotics are unable to reach the bradyzoites in adequate concentrations [23,27].
Toxoplasmosis prevention is centered around avoidance of contact with sources of infection, such as cats, contaminated environment, consumption of raw or undercooked meat, personal hygiene, and regular handwashing [23]. The control of mechanical vectors of transmission, such as cockroaches, flies, or rodents in the surroundings, can also be adopted in disease control [24].

2. Toxoplasma gondii Infections in Animals and Humans in Southern Africa

Toxoplasma gondii is a coccidian cosmopolitan parasite of global economic and zoonotic importance. The importance of T. gondii in the meat industry and public health has been reported in a wide variety of hosts and humans, especially among immunocompromised individuals. There is limited information on the distribution of T. gondii in animals and humans in southern African countries. The overall pooled prevalence is estimated as 17%.

The overall pooled prevalence of T. gondii infection 29% (95% CI: 7–54%) in domestic felids observed is lower than the pooled seroprevalence of 51% (20–81%) reported in Africa, 52% (15–89%) in Australia [10], and 30–40% global prevalence from previous studies [64,65]. However, the pooled prevalence of T. gondii infections observed in wild felids 79% (95% CI: 60–94%) is higher than the pooled prevalence reported in Africa, Asia, Europe, and South America [10], while in north African countries, no data were available on wild felids [66]. The role of felids (domestic and wild) in T. gondii epidemiology has been documented in several reports [10,67,68]. In this review, seven (7) studies were on wild felids, while five (5) studies were on domestic cats. A single infected felid is capable of shedding millions of oocysts for 10–15 days, thereby contaminating the environment and posing infection risk to various intermediate hosts [68]. Emphasis on the adequate veterinary care of animals, including frequent treatment of cats for toxoplasmosis and reduction in the population of stray cats in the environment, should be encouraged in southern African countries. Moreover, a surveillance system for Toxoplasma infection should be instituted at the wildlife-livestock interface areas in the region.

Limited studies exist on T. gondii infection in canids (domestic and wild), with an overall pooled prevalence of 69% (95% CI: 38–96%). This result is higher than the prevalence of 51.2.% reported in wild canids by Dubey et al. [69] and the global prevalence of 39.6% reported in foxes [70]. The studies in cattle were few and only done in South Africa and gave an overall pooled prevalence of 20% (95% CI: 5–39%), which is higher than the pooled prevalence of 16.3% (10.6–23.0%) from West Africa [71] and 12% (CI 8–17%) in the entire continent of Africa [1]. The estimated prevalence is, however, lower than the reported seroprevalence from Brazil and Sudan [72,73]. Studies have identified the consumption of raw or undercooked beef as a possible risk of toxoplasmosis transmission in humans [74,75].

Similarly, there is evidence of T. gondii infection in small ruminants (sheep and goats) [75], and the pooled prevalence of 11% (95% CI: 0–31%) recorded is lower than that of 29.1% (15.6–44.8) in sheep and 18.1% (4.0–38%) in goats in West Africa [71] and sheep 26.1% (95% CI: 17.0–37.0%) and goats 22.9% (95% CI: 12.3–36.0%) in Africa [1]. Among livestock species, sheep constitutes an important source of animal protein as well as meat and milk from goats [76], whereas consumption of rare lamb and drinking of unpasteurized milk has been identified as risk factors in acute toxoplasmosis transmission in humans [75,77,78,79].

Studies reporting the seroprevalence of T. gondii in pigs in southern Africa emanated from South Africa and Zimbabwe, with an overall pooled prevalence of 13% (95% CI: 1–29%). This is similar to the prevalence reported in pigs from Europe [80] but lower than the prevalence reported in pigs from North America, South America, Asia [80], West Africa [71], Africa [1], and globally [78]. Pigs are among the popular food animals and have been reported as a source of human toxoplasmosis through ingestion of raw or undercooked pork [81]. Toxoplasma gondii infections in pigs are either acquired prenatally via transplacental transmission or postnatally via ingestion of oocysts from a contaminated environment [1]. Hence, indoor rearing of pigs is important to reduce the exposure of pigs to T. gondii infections from the contaminated environment [1,43,82].

The overall pooled prevalence of 22% (95% CI: 0–84%) of T. gondii seroprevalence from chickens and birds in southern African countries is lower than the estimated prevalence of anti-T. gondii antibody 22% (95% CI: 0–84%) reported in chickens in West Africa [71] and 37.41% (95% CI: 29.20–46.00%) from chickens in Africa [1]. Chicken meat is a key contributor to animal protein due to affordability and availability [83]; however, it also plays a major role in human toxoplasmosis transmission when the meat is consumed raw or undercooked [1]. The free-range chickens ingest T. gondii oocysts from the contaminated environment while foraging, thus acting as zoonotic agents of human toxoplasmosis. The role of birds, especially the birds of prey, in maintaining transmission between the sylvatic cycle and domestic cycle has also been documented [84].

The pooled seroprevalence of anti-T. gondii antibody from humans came from studies that focused mainly on immunocompetent individuals, HIV+ patients, and pregnant women [8,54,57,60,62,63] as well as a few studies on blood donors and children [56,61]. Overall, the pooled prevalence of 14% (95% CI: 5–25%) of T. gondii infection in humans from southern African countries was lower than the seroprevalence reported from a meta-analysis conducted on pregnant women in African regions, American regions, eastern Mediterranean regions, Europe, the South-East Asia region, globally [85], and in some North African countries (Tunisia, Egypt, and Morocco) [66]. However, this prevalence is greater than the seroprevalence reported from Western pacific region and the World Health Organization (WHO) regions of the world, 1.1% (0.8–1.4) [85]. Humans acquire T. gondii infections either through ingestion of oocysts from the contaminated environment [86,87], via tissue bradyzoites from consumption of raw or undercooked infected meat, transplacental transmission from mother to fetus [31,88], or organ transplants or blood transfusion [11,89]. Infections in immunocompetent individuals are not associated with critical symptoms compared to the immunosuppressed, particularly AIDS patients or newborns. Congenital transmission often results in clinical manifestations, such as encephalitis, pneumonia, and ophthalmologic disorders [1,66].

3. Recommendation

Considering the limited information on the prevalence of T. gondii in southern African countries, more studies targeting the epidemiology of this parasite in the environment (soil and water), vegetable, food animals, wild animals, and humans (children, pregnant women, immunocompromised, and healthy people) must be conducted to better understand the transmission dynamics in the region. Additionally, there is a need to establish a surveillance system at the wild animals-livestock interface for monitoring transmission between livestock, wildlife, and humans. Furthermore, emphasis should be focused on health education and the preventive measures of toxoplasmosis, which include adequate cooking of meat, washing of fruits and vegetables before eating, and provision of potable water.

This entry is adapted from the peer-reviewed paper 10.3390/pathogens11020183

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