What Animals Are Known To Be Intermediate Hosts For Toxoplasma

Toxoplasmosis is a disease of significant health business concern for humans, livestock, and wild animals (Canfield et al., 1990; Epiphanio et al., 2001; Dubey, 2009a, 2016). The disease is caused by the true cat-borne protozoal parasite Toxoplasma gondii. Felids are the definitive host of the parasite and shed the oocyst stage in their feces, predominately following their first infection (Zulpo et al., 2018). Oocysts are particularly resistant to environmental conditions and tin remain infective for at least 18 mo under favorable weather, only they tin can be killed speedily via desiccation (Yilmaz and Hopkins, 1972; Frenkel et al., 1975; Dubey, 1998). Intermediate hosts of T. gondii can be any endotherm, which become infected via two major routes of transmission, oocyst or bradyzoite consumption (Aramini et al., 1999; Hill and Dubey, 2002; Dubey, 2016; Zulpo et al., 2018). Accordingly, based on the major routes of T. gondii manual to intermediate hosts, nosotros would expect the parasite's infection force per unit area to exist largely dependent on oocyst contamination in the surroundings. Similarly, oocyst contamination in the environment should be dependent on true cat density, environmental conditions, and the prevalence of T. gondii infection in the cat population (Frenkel and Dubey, 1973; Dubey, 1998, 2009b; Zulpo et al., 2018).

Many studies accept shown that ecological or physiological characteristics of an intermediate host species, such as age or body mass, can influence T. gondii seroprevalence (Afonso et al., 2007; Tagel et al., 2019). All the same, the relative contribution of T. gondii infection pressure to explaining seroprevalence in intermediate host species is not well known. This has important ramifications for the mitigation of T. gondii infection via reductions in infection pressure.

We investigated if T. gondii infection pressure level is sufficient, by itself, to explain the observed seroprevalence in intermediate host species. We defined T. gondii infection force per unit area to intermediate hosts equally the combined influence of cat density, environmental conditions, and the seroprevalence of the parasite in the cat population. If T. gondii infection pressure is sufficient to drive seroprevalence in intermediate host species, then we would wait that seroprevalence will scale with infection pressure for all species tested. If the relationship between T. gondii seroprevalence and infection pressure is linear, whereby an increase in infection pressure results in a proportional increase in seroprevalence, and then the proportional differences in seroprevalence among species will remain constant across regions of differing infection pressure.

To accost this question, nosotros sampled and tested business firm mice (Mus muscle) and bush-league rats (Rattus fuscipes), and we collated recently published information on T. gondii seroprevalence in koalas (Phascolarctos cinereus), tammar wallabies (Macropus eugenii), western grayness kangaroos (Macropus fuliginosusouth), and sheep (Ovis aries) from a region of low infection force per unit area and an adjacent region of high infection pressure (Taggart et al., 2019b, 2019c, 2020b). Nosotros obtained T. gondii seroprevalence estimates for all species and tested for effects of infection pressure, species, and their interaction on T. gondii seroprevalence. Hither, nosotros discuss the role of T. gondii infection pressure in driving seroprevalence in intermediate host species and the implication of this effect for mitigating T. gondii infection via reductions in infection force per unit area, and we hypothesize other factors that may contribute to the observed results.

MATERIALS AND METHODS

Study sites

Study regions included the Fleurieu Peninsula (35°35′xviii.96″S, 138°eleven′54.96″E) on mainland South Australia and the next Dudley Peninsula on Kangaroo Isle (35°48′v.four″S, 137°58′30.72″E). Both regions experience similar Mediterranean climates (Jenkins, 1985; Schwerdtfeger, 2002) and comprise similar state uses and vegetation types (cropping and pasture land interspersed with patches of native vegetation, largely depression Eucalyptus spp. woodlands). These 2 regions are located just 13.5 km apart. This assisted in controlling for whatsoever potentially misreckoning climatic conditions that may contribute to the differential survival of T. gondii oocysts in the environment, and consequently differences in T. gondii seroprevalence in our study species. Cat (Felis catus) abundance on the Fleurieu Peninsula, South Australia, is reported to be approximately x times lower than that on the adjacent Kangaroo Island (Bengsen et al., 2011; Taggart et al., 2019a; Hohnen et al., 2020). Similarly, the seroprevalence of T. gondii in cats on the Fleurieu Peninsula would be expected to be lower than that in insular cats, based on its lower seroprevalence in cats from the wider Australian mainland and the known high seroprevalence in insular cats (89.4% seropositive) (O'Callaghan et al., 2005; Fancourt and Jackson, 2014). Nosotros, therefore, assumed the Fleurieu Peninsula to be a region of low T. gondii infection pressure and Kangaroo Island to be a region of high T. gondii infection pressure. This assumption is supported by previous work, which has shown a lower seroprevalence of T. gondii in sheep (x%) on the S Australian mainland relative to that on Kangaroo Island (sheep 23%) and a depression seroprevalence of T. gondii in rabbits from this region likewise (O'Donoghue et al., 1987; McKenny et al., 2020; Taggart et al., 2020b). Future, we refer to the Fleurieu Peninsula on the South Australian mainland as a region of low T. gondii infection pressure level (low true cat abundance, expected low seroprevalence in cats) and Kangaroo Isle as a region of high T. gondii infection pressure (loftier cat abundance, loftier seroprevalence in cats).

We sampled house mice and bush rats at 4 sites in the region of depression T. gondii infection pressure and 4 sites in the region of high T. gondii infection pressure. Study sites within each region were a subset of the same study sites used to appraise cat abundance in each region in Taggart et al. (2019a). These sites were chosen to be representative of the remnant vegetation types in these regions and were all surrounded by agricultural grazing land.

Animal capture

House mice and bush rats were trapped in cages or Elliot traps baited with peanut butter and rolled oats, or in unbaited pitfall traps. Traps were deployed forth linear transects within native vegetation patches at intervals of 20 m. Trapping occurred between Jan 2017 and April 2018.

Blood sampling and processing

We collected blood from conscious house mice via venipuncture of the facial vein (Francisco et al., 2015) and from anesthetized bush rats via jugular venipuncture (Parasuraman et al., 2010). All captured rodents were marked to facilitate the identification of recaptures and to avoid individuals being sampled multiple times.

Blood samples were centrifuged, and sera samples were nerveless and stored at –20 C as described by Taggart et al. (2019c). Sera samples experienced ii freeze/thaw cycles earlier testing. Long-term sera storage does not significantly modify the interpretation of T. gondii serology (Dard et al., 2017).

Toxoplasma gondii antibiotic examination

Sera samples were tested for T. gondii immunoglobulin G (IgG) antibodies using equivalent methods for all individuals and species (Taggart et al., 2019b, 2019c, 2020b). We used a commercially available modified agglutination test (MAT) (Toxo-Screen DA, bioMérieux, Marcy-l'Étoile, France) every bit described in detail by Taggart et al. (2019c). The MAT is based on the directly agglutination of fixed T. gondii tachyzoites of the RH strain, with sera pre-treated with two-mercaptoethanol to neutralize IgM antibodies (Desmonts and Remington, 1980; Dubey and Desmonts, 1987). IgG antibodies typically take greater than ane wk to develop, but one time developed, they persist for the balance of the fauna's life. Consequently, this exam may requite false-negative results within the showtime week of infection (Dubey and Crutchley, 2008). Sera were screened at one:xl and 1:4,000 dilutions and classified as positive if agglutination occurred at either dilution. This minimized possible type two fault due to the prozone effect. With each assay, we included positive and negative control sera from known infected (intra-peritoneal inoculation with T. gondii tachyzoites) and uninfected mice and a negative phosphate-buffered saline (PBS, pH vii.2) control. A serum sample was classified every bit positive when agglutination of T. gondii formed a mat roofing nearly half or more of the well base.

The MAT has non been evaluated in the study species, only we assumed its diagnostic sensitivity and specificity to be satisfactory based on advisable quality controls and the high sensitivity and specificity of the assay reported in other species (Mainar-Jaime and Barberan, 2007). To our knowledge cross-reactivity with the MAT is low (Dubey, 2016; Gondim et al., 2017).

Data analysis

Collated information: We combined our data on T. gondii seroprevalence in house mice and bush rats with previously published data on T. gondii seroprevalence in koalas, tammar wallabies, western grayness kangaroos, and sheep (Taggart et al., 2019b, 2019c, 2020b). All of these species were sampled within a 2-yr period and tested using equivalent methods from the described regions of low and high infection pressure (Taggart et al., 2019b, 2019c, 2020b). House mice, bush rats, koalas, and western grey kangaroos were sampled in the same regions of low and high T. gondii infection pressure. Tammar wallabies and sheep were only sampled from the region of high T. gondii infection pressure.

Statistics: We used generalized linear models (GLMs) to investigate the association between T. gondii seroprevalence and the predictor variables infection pressure level (depression vs. loftier) and species, and their interaction. In each GLM, T. gondii seroprevalence in an animal was treated as a binary response, and the default logit link was used. Statistical significance was adamant using a score examination (Lagrange multiplier) and model parsimony assessed using the Akaike information criterion (AICc). We considered a model to take substantial support if P values for predictor variables were <0.05 and ΔAICc was <2 (Burnham and Anderson, 2002). Due to naught infections inside the region of low infection pressure level, the GLM exhibited quasi-complete separation, and so the conventional Wald's exam was not useful for posthoc comparisons betwixt species within locations (Mansournia et al., 2018).

Given this separation effect and the finding that at that place were highly significant species effects in our GLM (see Results), nosotros compared T. gondii seroprevalence between species within the region of high infection pressure only. For each two × 2 cross-tabulation of counts of 2 species by T. gondii seropositivity, we used either a Fisher'south exact test or chi-squared exam with the (n – one) adjustment (Campbell, 2007), depending on the count of positive animals in the groups being tested. To correct for multiple comparisons, we determined statistical significance co-ordinate to a Bonferroni adjusted blastoff value of 0.003. However, we acknowledge that this correction will exist conservative due to known dependence between tests (Abdi, 2007). We present T. gondii seroprevalence and binomial verbal 95% confidence intervals. All statistical analyses were performed in base of operations R version R iii.5.1 (R Core Team, 2020).

RESULTS

We sampled 19 mice and 169 rats in the region of depression infection force per unit area and 36 mice and 46 rats in the region of loftier infection pressure, totaling 270 individuals (Table I). We additionally compiled T. gondii seroprevalence data on another 124 animals across another ii species from the region of depression infection force per unit area, and another 886 animals across another 4 species from the region of high infection pressure (Table I). The credible seroprevalence of T. gondii for both mice and rats from the region of depression infection pressure, and for mice from the region of high infection pressure was 0% (Fig. 1; Table I). From the region of high T. gondii infection pressure, a single rat was positive, giving an apparent seroprevalence of 2.2% (Fig. 1; Table I).

Tabular array I

Toxoplasma gondii seroprevalence (with 95% confidence intervals [CIs]) by species from a region of low infection pressure and a region of high infection force per unit area.

Figure 1.

Toxoplasma gondii seroprevalence estimates (with binomial 95% confidence intervals) by species from a region of low infection force per unit area (blue circles) and a region of high infection pressure (scarlet diamonds). Color version is available online.

Our most parsimonious GLM supported the inclusion of infection pressure level and species as fixed effects (infection pressure: Rao score = 16.84, df = 1, P ≤ 0.001; species: Rao score = 228.01, df = 5, P ≤ 0.001;  Suppl. Information, Table S1 (para-107-04-02_s01.docx)). The seroprevalence of T. gondii was substantially higher inside the region of loftier infection pressure level relative to that inside the region of low infection pressure, and large variation in seroprevalence existed betwixt species generally. The interaction infection pressure*species was not supported in GLMs due to the absence of T. gondii infection in all species within the region of low infection pressure level. Still, we found large variation in T. gondii seroprevalence amongst species within the region of high infection force per unit area using chi-squared and Fisher's exact tests (Table II). Inside the region of high infection pressure level, the seroprevalence of T. gondii in sheep was greater than the seroprevalence of T. gondii in all other species; similarly, the seroprevalence in kangaroos was greater than that in mice, rats, and koalas, and the seroprevalence in wallabies was greater than that in koalas. For all other pair-wise comparisons we plant no deviation in T. gondii seroprevalence according to our Bonferroni adjusted alpha value of 0.003. We did not test for differences in T. gondii seroprevalence between species within the region of low infection force per unit area because we observed no infection in whatsoever species and hence no variation in seroprevalence between species.

Tabular array Two

P values for the comparing of Toxoplasma gondii seroprevalence across species within the region of high infection pressure. Statistically significant comparisons are listed in bold format and were determined based on a Bonferroni adjusted alpha level of 0.003. Numbers in parentheses indicate χⁱⁱ values where a chi-squared examination was used for comparison instead of a Fisher's verbal exam.

Word

If T. gondii infection pressure is sufficient, past itself, to drive seroprevalence in intermediate host species, then seroprevalence must scale with infection pressure for all species. If this human relationship is also linear, then the proportional differences in seroprevalence among species will remain constant across regions of differing infection force per unit area. If intermediate host species seroprevalence scales with infection pressure, only proportional differences in seroprevalence among species are not constant across regions of differing infection pressure, so a sufficient, but not-linear, relationship between T. gondii seroprevalence and infection pressure will exist. However, if intermediate host species seroprevalence does not calibration with infection pressure, and then T. gondii infection force per unit area solitary cannot exist sufficient to drive seroprevalence, and seroprevalence must be strongly driven by other factors in addition to infection force per unit area. It is not possible for proportional differences in T. gondii seroprevalence among species to remain abiding across regions of differing infection pressure if seroprevalence does not scale with infection pressure.

Nosotros plant no prove of T. gondii presence within our region of low infection pressure. Consequently, we cannot be sure that our specific report sites on the Fleurieu Peninsula represented a region of low infection pressure and did non represent a region of no/zero infection pressure. This has implications for the testing and interpretation of the conditions necessary to demonstrate a sufficient, or sufficient and linear, relationship between T. gondii infection force per unit area and intermediate host seroprevalence.

When testing if infection pressure scales with seroprevalence, it is irrelevant if T. gondii actively circulates in our region of low infection pressure or not. For mice, rats, and koalas, we found no testify of a difference in T. gondii seroprevalence betwixt our regions of low and loftier infection pressure. Thus, for these three species, our data provide evidence that T. gondii seroprevalence does not scale with infection force per unit area and is not sufficient, by itself, to drive seroprevalence.

When testing if proportional differences in seroprevalence amid species remain constant across regions of differing infection pressure level, it is important that T. gondii actively circulates to some extent inside our region of depression infection force per unit area. If it does not, so our test of the presence of a linear relationship between T. gondii infection pressure and intermediate host seroprevalence is invalid. Although we cannot conclusively demonstrate that T. gondii does circulate at our specific study sites within our region of low infection pressure, nosotros suggest it is unlikely that T. gondii is completely absent from these study sites for the following reasons: (1) T. gondii antibodies have previously been detected in sheep, rabbits, and people on the broader Fleurieu Peninsula region, which encompasses our region of low infection pressure (Johnson et al., 1980; Berger and Gideon Informatics, 2010; Lanyon and O'Handley, 2020; McKenny et al., 2020); (2) our specific study sites within the region of low infection pressure are known to support a wild/feral cat population (Taggart et al., 2019a); (three) a recent systematic review and meta-analysis of T. gondii seroprevalence in felids worldwide and a regional review of T. gondii seroprevalence in cats in Australia both suggest that its seroprevalence in cats in Commonwealth of australia is among the highest worldwide (Fancourt and Jackson, 2014; Montazeri et al., 2020); (4) it is not uncommon for T. gondii seroprevalence values to be low, <1%, but notwithstanding T. gondii is still present and actively circulating (Dubey et al., 2006; Murata et al., 2018); (v) T. gondii is considered to be a ubiquitous parasite worldwide (Shwab et al., 2018); and (6) we are unaware of whatever studies that have demonstrated that T. gondii was absent-minded from locations with a known cat population, climatic weather conducive to the survival of oocysts in the surround, and known infections in multiple species within close proximity. If T. gondii does truly broadcast at our specific study sites on the Fleurieu Peninsula, and this region can truly be considered to be a region of low infection pressure, then our information would also advise that proportional differences in seroprevalence among species are not constant across regions of differing infection pressure, and infection force per unit area is not linearly related to seroprevalence in intermediate host species. This would be supported by the big divergence in T. gondii seroprevalence betwixt kangaroos and that in mice, rats, and koalas within the region of high infection pressure simply no difference in the seroprevalence experienced by these species within the region of depression infection pressure.

As we did not observe a consistently lower seroprevalence of T. gondii in intermediate host species inside the region of low infection pressure relative to the same species inside the region of high infection pressure, our data suggest that T. gondii infection pressure, while necessary, is just i of many factors that influences seroprevalence in an intermediate host species. Nosotros cannot be 100% confident if this human relationship betwixt T. gondii infection pressure level and intermediate host species seroprevalence is linear or not.

Our results have direct relevance to the mitigation of T. gondii infection via reductions in infection pressure, for example, via the removal of cats from an surround. Where T. gondii seroprevalence in an intermediate host species is already low, our results suggest that farther reduction in the infection force per unit area will not necessarily decrease seroprevalence in those species. Instead, our results suggest that reductions in T. gondii infection pressure, intended to reduce infections, may be nearly effective and applicable to species that are known to experience high rates of infection.

Our data raise 2 boosted questions. (i) In addition to T. gondii infection pressure level, what drives seroprevalence in intermediate host species within our sampled regions? (2) Are the sampled species of import to the epidemiology of T. gondii within the sampled regions? For kangaroos, wallabies, and koalas, T. gondii seroprevalence values and the importance of these species to the epidemiology of T. gondii within our sampled regions were discussed in detail by Taggart et al. (2019b) and Taggart et al. (2019c). However, rodent seroprevalence values are yet to exist discussed.

Both mice and rats in our study experienced a low seroprevalence of T. gondii, even within our region of known high infection pressure. Equally seroprevalence, in full general, is known to be driven by both the incidence of infection and elapsing of seroconversion in a species (Dohoo et al., 2009), information technology is likely that both ecological and physical traits of the mice and rats sampled contributed to the low T. gondii seroprevalence observed. Both of these species would exist expected to spend a large proportion of their time foraging at or beneath basis level and could therefore ingest T. gondii oocysts in contaminated soil (Gleeson and Van Rensburg, 1982). However, both species are small-scale, have modest total energy requirements, and consume small full volumes of food. This would be expected to reduce the incidence of infection that these species would experience (Afonso et al., 2007). Both species are as well short-lived (≤ane twelvemonth), may suffer mortality or morbidity from toxoplasmosis, or may take an increased chance of predation due to a reduction in their fear response from latent toxoplasmosis, all of which would be expected to reduce the duration of seroconversion that they experience (Matthewson et al., 1994; Dubey, 1996, 2006; White et al., 1996; Berdoy et al., 2000; Vyas et al., 2007; Boillat et al., 2020).

While in that location are several factors that make it logical for rodents to experience low T. gondii seroprevalence, large variability in seroprevalence in rodents is known to occur (Galeh et al., 2020). Our results are additionally consistent with others on islands where T. gondii infection pressure is known to exist high just low seroprevalence values have been recorded in local rodent populations (Dubey et al., 2006; Murata et al., 2018). This may suggest that loftier infection pressure combined with short species generation times may facilitate rapid evolution and bulldoze such species towards increased resistance to T. gondii infection and consequently a lower observed seroprevalence. While nosotros are non aware of evidence to this effect for T. gondii, we propose it would exist worthy of further investigation in lite of rapid evolutionary changes suggested in other species following intense selection pressures (Jolly et al., 2018; Jolly and Phillips, 2020).

Even in the instance that rodents feel a low T. gondii seroprevalence, recent simulations propose that rodents are even so highly important to the epidemiology of T. gondii due largely to the frequency with which they are consumed by felids (Taggart et al., 2020a). For example, the authors suggest that if felids consume an average of 1 rodent per twenty-four hour period, and then a T. gondii seroprevalence of but 0.2% (one/500 positive) in rodents volition crusade 51.9% of felids to be exposed to T. gondii annually.

Our study highlights the fact that T. gondii infection pressure is necessary, but not sufficient by itself, to explain seroprevalence in intermediate host species. This suggests that seroprevalence is strongly driven by factors other than infection force per unit area. When seroprevalence is already depression, reductions in infection pressure may not accomplish whatsoever farther noticeable reduction in seroprevalence. Rather, reductions in T. gondii infection pressure intended to reduce infections may be nigh effective and applicable to species that are known to experience high rates of infection.

Source: https://bioone.org/journals/journal-of-parasitology/volume-107/issue-4/21-28/Infection-Pressure-is-Necessary-but-not-Sufficient-by-Itself-to/10.1645/21-28.full

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