Recent aspects on epidemiology, clinical disease, and genetic diversity of Toxoplasma gondii infections in Australasian marsupials

Abstract

Background Toxoplasma gondii infections are common in humans and animals worldwide. Among all intermediate hosts of T. gondii, captive marsupials from Australia and New Zealand are highly susceptible to clinical toxoplasmosis. However, most free-range marsupials establish chronic T. gondii infection. Infected marsupial meat may serve as a source of T. gondii infection for humans. Differences in mortality patterns in different species of kangaroos and other marsupials are not fully understood. Lifestyle, habitat, and the genotype of T. gondii are predicted to be risk factors. For example, koalas are rarely exposed to T. gondii because they live on treetops whereas wallabies on land are frequently exposed to infection. Methods The present review summarizes worldwide information on the prevalence of clinical and subclinical infections, epidemiology, and genetic diversity of T. gondii infecting Australasian marsupials in their native habitat and among exported animals over the past decade. The role of genetic types of T. gondii and clinical disease is discussed. Results Fatal toxoplasmosis has been diagnosed in captive Australasian marsupials in Argentina, Chile, China, Germany, Hungary, Japan, Spain, Turkey, and the USA. Most deaths occurred because of disseminated toxoplasmosis. Genetic characterization of T. gondii strains isolated from fatal marsupial infections identified Type III as well as atypical, nonclonal genotypes. Fatal toxoplasmosis was also diagnosed in free-ranging wombats (Vombatus ursinus) in Australia. Genetic characterization of DNA amplified directly from host tissues of subclinical culled kangaroos at slaughter identified many mixed-strain infections with both atypical and recombinant genotypes of T. gondii. Conclusions Most Australasian marsupials in their native land, Australia and New Zealand, have high prevalence of T. gondii, and kangaroo meat can be a source of infection for humans if consumed uncooked/undercooked. The genotypes prevalent in kangaroos in Australia and New Zealand were genetically distinct from those isolated or genotyped from most macropods in the USA and other countries. Thus, clinical toxoplasmosis in marsupials imported from Australia is most likely to occur from infections acquired after importation. Graphic abstract

Additional evidence of tigers (Panthera tigris altaica) as intermediate hosts for Toxoplasma gondii through the isolation of viable strains

“…Therefore, striated muscle, spleen, kidney liver, lungs, and brain could be selected to isolate T. gondii . This finding is consistent with other reports on cats or macropods ( Dubey et al, 2020 , 2021 ). Parasite load may be related to animal species, infection status, strain, or genotypes of T. gondii and the environment.…”

Acute Disseminated Toxoplasmosis in Two Specimens of Macropus rufogriseus Caused by a Genotype so far Exclusive to South America

“…This is the first time that this genotype is reported in macropods, and, given the histopathological findings, it could be considered virulent for this species. Although the isolate had a majority of type III alleles for the 10 standard markers, and type III alleles are considered to have low virulence in mice, a clonal type III caused disseminated toxoplasmosis and death in M. rufus, M. rufogriseus and M. eugenii from Argentina and the USA ( 26 , 27 ).…”

“…Even though these two wallabies were treated with Sulfadoxine/Trimethoprim and Clindamycin, they were not effective, and both animals died. Currently none of the treatments described to treat toxoplasmosis in macropods has proven to be effective and the variability of the treatment response could be subject to the specific genotype that caused the clinical signs ( 8 , 27 ). It has been suggested that the exhibits of macropods and other susceptible species must have a good water drainage, in order to avoid water stagnation and prevent storm water (that could be carrying oocysts) from running into the exhibits ( 8 ).…”

Imaging Diagnosis: Thoracic radiographic features of toxoplasmosis in a 14‐month‐old Red Kangaroo (Macropus rufus)

“…It has been speculated that since Australian marsupials evolved in the absence of cats they therefore are thought to be more susceptible to toxoplasmosis 2 . Vertical transmission has also been proven to occur in marsupials, though infections in the joey may be subclinical 3,9 . It has also been shown that those that are immune compromised or stressed can have increased susceptibility to clinical manifestation of the disease.…”