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The Life Cycle of Toxoplasma gondii
in the Natural Environment
Emmanuelle Gilot-Fromont, Maud Lélu, Marie-Laure Dardé,
Céline Richomme, Dominique Aubert, Eve Afonso,
Aurélien Mercier, Cécile Gotteland and Isabelle Villena
Additional information is available at the end of the chapter
http://dx.doi.org/10.5772/48233
1. Introduction
Toxoplasma gondii (T. gondii) is considered as one of the most successful parasites in the
world. This success is first illustrated by its worldwide distribution, from arctic to hot desert
areas, including isolated islands and in cities [1]. T. gondii is also among the most prevalent
parasites in the global human population, with around one third of the population being
infected [2]. Finally, it is able to infect, or be present in, the highest number of host species:
any warm-blooded animal may act as an intermediate host, and oocysts may be transported
by invertebrates such as filtrating mussels and oysters [1, 3].
Beyond this ubiquitous distribution lies a fascinating transmission pattern: simply saying
that T. gondii has a complex life cycle does not encompass all transmission routes and modes
that can be used by the parasite to pass from definitive hosts (DHs), where sexual
reproduction occurs, to intermediate hosts (IHs). The “classical” complex life cycle uses
felids (domestic and wild-living cats) as DHs and their prey as IHs (Figure 1). Felids are
infected by eating infected prey and host the sexual multiplication of the parasite. They
excrete millions of oocysts that sporulate in the environment. Sporulated oocysts may
survive during several years and may disperse through water movements, soil movements
and microfauna. Ingesting a single sporulated oocyst may be sufficient to infect an IH and
begin the asexual reproduction phase [1]. This classical life cycle thus relies on a prey-
predator relationship and on environmental contamination, like other parasites, e.g.,
Echinococcus multilocularis [4].
However, beside this classical cycle, T. gondii shows specific abilities that allow it to use
“complementary” transmission routes (Figure 1). During the phase of asexual
multiplication, tachyzoites may disseminate to virtually any organ within the IH, in
Toxoplasmosis – Recent Advances
4
particular to muscles, brain, placenta, udder and gonads. Asexual forms are then infectious
to new hosts, thus direct infection among IH is possible by several routes which
epidemiological importance has to be discussed: vertical transmission through the placenta,
pseudo-vertical transmission through the milk, and sexual transmission through the sperm
[1, 5, 6]. In humans, T. gondii may also be transmitted during blood or organ transplant.
Finally, the infectivity of asexual forms towards new IHs entails the ability for the parasite
to be transmitted among IHs by carnivory. This transmission route is estimated to cause the
majority of cases in humans [7], although people may also get contaminated by ingesting
oocysts after a contact with contaminated soil, water, vegetables or cat litter. All the possible
transmission routes among IH make the parasite able to maintain its life cycle, at least
during a few generations, in the absence of DH and without environmental stage [8].
Moreover, at a high dose, oocysts from the environment may also be infectious for DHs [9],
thus the parasite may bypass the IH and use a DHs-environment cycle. The infectivity of
oocysts towards cats is relatively low thus the importance of this cycle may be questioned
[10]. However, taken together, these observations suggest that T. gondii may theoretically
have two distinct life cycles, one among IHs and the other one between DHs and
environment.
Figure 1. Life cycle of Toxoplasma gondii: the “classical” life cycle between intermediate hosts (IH,
rodents), definitive hosts (DH, felids) and environment (E, soil) is represented with large arrows, while
the “complementary” transmission routes (vertical or horizontal transmission among IHs and
environment-to-cat transmission) are represented with small arrows.
Moreover, in IHs, the infection of the brain results in several specific clinical manifestations,
modifications of host behaviour and life history that influence transmission. As a result of its
presence in the brain of IHs, T. gondii manipulates host behaviour in two ways, by
specifically increasing attractiveness of cat odours to rodent IHs, thus favouring
transmission from IH to DH [5, 11], and by increasing the sexual attractiveness of infected
males, which favours sexual transmission [6].
These numerous capacities of transmission clearly allow T. gondii to be distributed
worldwide. However, this does not mean that the risk of toxoplasmosis is identical
everywhere. On the contrary, a highly structured pattern of infection can be demonstrated,
for example by comparing the level of infection of different human populations. Among
The Life Cycle of Toxoplasma gondii in the Natural Environment 5
countries, nationwide seroprevalences in women of childbearing age vary from less than
10% to more than 60% [12]. Within countries, a strong variability is also present: in France,
the incidence of T. gondii varies from 1 to 68 cases per 1000 pregnancies among the 22
metropolitan regions [13]. Finally, spatial heterogeneity is also present at a more local scale,
for example among districts within a region, and up to the level of families: within a village,
individuals of the same family tended to have identical serological status [14]. Due to this
heterogeneous distribution, the burden of toxoplasmosis and the associated socio-economic
cost are unevenly distributed. Elucidating the causes of this distribution of T. gondii is
necessary to improve prevention. However, this proves to be a difficult task, as the variability
of parasite prevalence may reflect variations in many aspects of the life cycle. For example,
considering the “classical” cat-environment-prey life cycle, the transmission from IH to DH
likely depends on the level of predation of DHs on IHs, thus on the presence and densities of
DHs and IHs, as well as on the diet of DHs. The survival of oocysts is influenced by
temperature, moisture and UV radiation, thus should be determined by the meteorological
conditions prevailing in the area, while dispersal depends on soil and water movements, as
well as on the accumulation in invertebrates. The complementary routes of infection depend
on the presence of omnivorous species (carnivory), the population dynamics of IH
populations (vertical transmission) and the social structure (sexual and milk transmission).
In this chapter we aim to provide a comprehensive overview of factors that are recognized
or can be expected to determine T. gondii dynamics in animal populations and in the
environment, which constitute the reservoir of human infection, i.e., a set of
epidemiologically connected populations and environments in which the pathogen can be
permanently maintained and from which infection is transmitted to the defined target
population [15]. Although the risk for people is largely due to the quality and intensity of
their contacts with this reservoir, here we only deal with variations of the cycle in the
environment and in animals. We summarize which mechanisms are now established and
identify areas where data are lacking. We first show that the dynamics of the life cycle varies
according to the relative densities of IHs and DHs, in particular along the urban-rural-wild
gradient. Then we detail the variations observed in each of these environments at different
spatial scales, and the factors that have been found to influence transmission dynamics. We
conclude on how the variations described here should affect human exposure and should be
considered for prevention.
2. The urban- rural-wild gradient
The life cycle of T. gondii is dependent on populations of IHs and DHs, and on the level of
predation between them. These ecological determinants are themselves dependent on their
environment. Because humans exert a major influence on the structure of their environment,
the first structuration of these IH-DH communities comes from the urbanization gradient.
We first explicit how IHs and DHs populations vary along this gradient before detailing
how these variations affect the dynamics of T. gondii.
Toxoplasmosis – Recent Advances
6
2.1. Host densities and predation rates vary along a urbanization gradient
Taking advantage of a high adaptability and following human migrations, the domestic cat
Felis catus has colonized a wide variety of habitats, ranging from urban areas to non-
anthropized islands, through, agricultural areas, arid or semi-arid areas, villages or cities,
from polar to equatorial climatic regions [16]. However, due to the behavioural plasticity of
this species, population density and structure vary, depending on the abundance and
distribution of food resources and shelters [16, 17]. In particular, cat populations are
structured differently along an urban-rural-non-anthropized (“wild”) gradient (Figure 2).
The highest densities of cats are found in urban populations of stray cats locally more than
1000 cats/ km² [18, 19]. At these high densities, cats form large multimale–multifemale social
groups and share their territory, as well as available resources [16]. Most resources are
provided directly or not, by people (feeders, garbage) [19]. In rural areas, population density
is moderate (100-300 cats/ km²) [20, 21, 22]. Most cats have an owner who provides food and
shelter but cats are generally free to roam [23]. An important part of cats diet result from
predation: 15 to 90% depending on cat lifestyle [24, 16]. In rural areas, the spatial
distribution of cats is based on human settlements: the social groups are based on a house or
farm that provides most of the feeding and nesting resources. Around a feeding point, cats
may form groups of up to 20 individuals, often constituted by related females and their
kittens [16]. In fact, in such areas, a gradient can be observed between pet-owned cats
mostly fed by the owner, to farm cats and feral cats mostly living on predation. Finally, feral
cats occupying non-anthropized areas (sub-Antarctic, arid or forested areas), survive
exclusively through predation, live at low density (1 to 10 cats/ km²), in large and non-
overlapping home ranges [25, 26].
Rodent densities also vary along the urban-rural-wild gradient (Figure 2). However,
comparisons are not straightforward since many species are concerned and most of them are
not present in all environments. The available estimates suggest that some species may live
at very high densities in agricultural landscapes: for example, common voles Microtus arvalis
and water voles Arvicola terrestris may reach 100 000 individuals/km² [27]. In contrast, in
urban areas, the density of wood mice Apodemus sylvaticus was estimated to lie around 2 000
- 8 000 mice/km² [28, 29].
The third parameter that varies along the urban-rural-wild gradient is the rate of predation
of rodents by cats, i.e., how many rodents does a cat ingest per unit of time. This parameter
is crucial for the transmission of T. gondii from IH to DH: combined with the prevalence in
prey, it determines the risk for a cat to get infected. The importance of the predation rate is
illustrated by the finding that cats with frequent outdoor access show higher predation rates
[16] and higher prevalences than cats not allowed to roam [30, 31, 32, 33, 34]. The predation
rate depends on the availability of rodents, i.e., on the density of rodents relative to cats, and
on the availability of other food resources provided by people. The predation rate is lowest
in urban populations, ranging from 10 to 27 prey/cat/year [35, 36, 37]. For suburban and
rural sites, estimated values for predation rates range from 21 to 436 prey/cat/year [10, 24,
38, 39]. Finally, the predation rate should be highest in non-anthropized areas, where cat
exclusively live on predation.
The Life Cycle of Toxoplasma gondii in the Natural Environment 7
Figure 2. Variations of human density and anthropogenic food supply, cat density, rodent density and
predation along an urban-rural-wild gradient. The magnitude of the bars represents the relative
importance of each factor according to the degree of urbanization (modified from [4]).
Because of these variations of three key parameters of T. gondii cycle (densities of DHs and
IHs, and predation rate), one can hypothesize that the dynamics of T. gondii should vary
qualitatively and quantitatively along the urban-rural-wild gradient, following the specific
features regarding T. gondii transmission in each environment. Urban areas, at least in the
limited areas where cats live, support the highest densities of DHs. However, in cities,
rodent densities are relatively low and predation rate is low due to the availability of
anthropogenic food resources. The transmission through predation is not expected to be
favoured in this case, but the DH-environment cycle should be maximized. On the contrary,
in the wild environment, the level of predation of cats on rodents is maximal, but cat density
is low, thus transmission should occur only by predation. Finally, rural areas combine
intermediate to high values of IH and DH density, with high predation rates. Thus these
may be the most favourable for the transmission of T. gondii [40]. This transmission should
occur largely through “classical” IH-DH transmission, but transmissions among IHs and
through a possible DH-environment cycle should also be possible in this case.
2.2. Variations in T. gondii dynamics along the urban-rural-wild gradient
The hypothesis that the dynamics of T. gondii transmission varies along the urban-rural
gradient has been tested through a theoretical approach, using an epidemiological model
[10]. The aim was to estimate the contributions of the IH-DH and DH-environment cycles in
the spread of T. gondii according to the predation rate, with stable cat population size. The
modelling approach allowed the authors to compare populations differing only by the rate
of predation, all else being equal. The model first confirmed that the rural environment
(here defined as having predation rates above 21 prey/cat per year [35, 36] is favourable for
T. gondii, as transmission increases with the predation rate [10]. Seroprevalences predicted
for cats ranged from 33.2 to 83.4% in the rural environment vs. 6.9 to 33.2% in urban areas.
Moreover, in rural-type areas, the contribution of the IH-DH cycle increases with the
predation rate, and may reach 70% of the transmission (Figure 3). The DH-environment
cycle may theoretically be responsible for more than 50% of the transmission, but only in
extremes cases with predation rates lower than 9 prey/cat/yr (Figure 3). It is noteworthy that
Toxoplasmosis – Recent Advances
8
the predicted prey seroprevalences, from 2.4 to 5 % along the gradient, was always low
compared to the magnitude of cat seroprevalences.
The cat serological prevalences predicted by [10] agree with values observed along the
urban rural gradient: when natural populations (as opposed to heterogeneous samples
constituted from veterinary clinics or facilities) are considered, seroprevalences are clearly
lower in urban (between 15 % to 26% [41, 33, 34, 42, 43]) than in rural areas (48% to 87.3%
[44, 30, 45, 32, 42]). They also reach high values in non–anthropized areas: 51% in Kerguelen
island [46]. In rodents, prevalence is generally low (0 – 10% [47, 46]), which renders
comparisons difficult. High seroprevalences have been occasionally reported in brown rats
(70% in Italy [48]) and in house mice (59% in rural and sub-urban areas in England [49]).
However, these limited data do not permit to draw a clear pattern among environments in
rodents. Interestingly, the usually low rodent seroprevalences are in accordance with
predictions of the model [10]. The model also suggested that cat seroprevalence is less
dependent on prey seroprevalence than on predation rates and prey availability. Thus
obtaining accurate estimate of these two last parameters should be more important to
understand T. gondii epidemiology than estimating rodent seroprevalence.
Figure 3. Contributions of the DH-Environment and IH-DH cycles in the basic reproductive rate R
0
of T. gondii
according to the predation rate of IHs by DHs. Predation rates below 27 prey/cat per year represent urban areas,
values above 21 prey/cat per year represent rural areas. Modified with permission from [10].
The last way to compare environments would be to compare the levels of soil contamination
among environments. However, estimating the level of environmental contamination
requires information on the number of new infections in cats (incidence) through
longitudinal studies. Based on serological follow-up of cats, incidence was estimated to 0.26-
0.39 infections/cat per year in three rural populations located in France [32]. Incidence was
also estimated in one urban site (0.17 infections/cat/year [50]) and in one population living in
a non-anthropized environment [46], using the age-seroprevalence relationship. Using data
The Life Cycle of Toxoplasma gondii in the Natural Environment 9
on oocyst shedding, Dabritz et al. [51, 52] estimated that 0.04 infections could occur per cat-
year in cats recruited through local veterinarians in coastal cities in California (USA).
Incidences estimates may be combined to local cat densities, in order determine the number
of infection that could occur each year in a given site. In urban sites, even if incidence is low,
very high densities of cats lead to expect a high number of infections: 165 infections per km²
per year could occur in the dense population studied by Afonso et al. [41, 50]. In rural sites
where cats live in density varying between 120 and 200 cats per km², [32] estimated that 31
to 72 infections per km² per year could occur. In Kerguelen, where incidence is high but
density is only 1-3 cats/km2, the number of new cases per year would be only around
1/km2/year. Based on the assumption that primary infected cats shed between 1 and 50
millions of potentially infectious oocysts in the environment, oocyst burden may be
estimated in each case, as was proposed for rural populations [32]. The results of the cited
studies are summarized in Table 1, to give a range of possible estimates for oocyst burden.
This may be compared to the estimate from a recent study on owned cats living in coastal
California: [51] estimated that the annual burden of oocysts in the environment ranged
between 94 and 4671 oocysts/m².
The urban-rural-wild gradient is thus a key determinant of the T. gondii dynamics. The
general level of transmission varies along this gradient, rural areas being particularly
favourable for T. gondii transmission. Moreover, the relative importance of different
transmission routes is not equivalent along this gradient. In particular, the DH-environment
cycle may become significant at very low levels of predation rate, especially in urban areas.
These variations are expected to influence the risk for other target species, and especially for
people, to get infected. In particular, generally speaking, the level of soil contamination is
expected to be highest in the areas where urban feral cats are concentrated, and lowest in the
wild environment. However, with each environment, spatial and temporal heterogeneities
are present. They will be detailed in the following paragraphs.
Population Kerguelen
(Non-anthropized)
Aimargues, Saint-
Just Chaleyssin,
Barisey
(Rural)
Lyon Croix-
Rousse
(Urban)
Seroprevalence in cats (%) 36.2 – 55.0 47.4 – 55.1 18.6
Incidence in cats (number
of new infections/cat/year) 0.28 – 0.65 0.26 – 0.39 0.17
Number of new cat
infections/km2 0.66 – 1.3 31 - 72 165
Oocyst burden (number
deposited /year/m2) 17 - 33 775 - 1800 4125
Table 1. Estimated levels of contamination by oocysts in five populations located in different
environments. The table summarizes the studies of one population in a non-anthropized island (2 study
sites) [46], three rural populations [32] and one urban population [41]. Oocyst burdens are estimated
considering that an infected cat produces 25 millions oocysts.
Toxoplasmosis – Recent Advances
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3. Urban toxoplasmosis
Urban landscapes are characterized by highly fragmented natural or semi-natural habitats
resulting in a mosaic of patches varying in size and quality. Dispersal abilities of animal
species between patches are generally affected by roads or by distance to the nearest patches
[53, 54]. Many animal species are thus restricted to parks, artificial forest fragments or
recreation areas [55]. This results in local extinctions, increased local population density, or
social disturbance. Natural populations of domestic cats are present in urban areas in
various sites including hospital gardens [56], parks [57, 58], cemeteries or squares [59],
taking advantage of the abundance of shelters, food wastes linked to human activity or food
provided by cat lovers [59, 17, 54]. Densities regularly exceed 250 cats per km² [16], and can
reach up to 2000 cats per km² like in urban parks in Italy [58].
In urban areas, rodent densities are heterogeneous and generally strongly related to
vegetation cover, predation pressure [29], and/or on how the presence of rodents is
controlled by trapping or poisoning. For example, the density of field mouse Apodemus sp.
can range from no individual in areas occupied by dense populations of predators, to 20,000
individuals per km² in isolated patches [28, 29]. Communities of small mammals can persist
at high density in small habitat patches sparsely settled by predators [28]. It is therefore
unlikely that cat and IHs populations coexist at high densities in the same habitat patches. In
addition, urban cats are attracted by food provided by humans, easily accessible all over the
year, and that requires no effort of predation. The presence of such a resource can reduce the
motivation to hunt in cats [16, 59]. Observations made on urban cats in hunting activity are
thus rare in such areas [41]. The altered predator-prey dynamics limits IH-HD T. gondii
transmission, however toxoplasmosis does occur in urban hosts. Most surveys conducted in
stray cats show low prevalences ranging from 5 to 20% [60, 61, 62, 41]. However, high values
have occasionally been found: 35.4% in Sao Paolo [62], 51.9 Barcelona [63], 70.2 in Ghent,
Belgium [64]. These cases may correspond to areas where cats have access to predation.
The high local densities of cats also entail a high local level of environmental contamination
by T. gondii oocysts. Beside density, in such areas, cats often use the same place to defecate
where they burry or expose their faeces as scent marks [16, 65], and a single location may be
used by several cats when cat density is high [66]. Moreover, this behaviour is expected to
favour the direct contamination of cats by oocysts while defecating, since oocyst load in
defecating areas is extremely high, and cats are exposed through scratching the soil, before
cleaning their paws and fur. These defecation sites spread over cat territory cumulate a high
concentration of oocysts in areas closed to humans. A study of a cat population living in the
Croix-Rousse hospital (Lyon, France) showed that defecation sites were the areas most often
found to be positive for T. gondii DNA, and may be viewed as hot spots of environmental
risk to humans [50]. Similarly, in Poland and in China, contaminated soil samples have been
found in public parks and sand pits [67, 68]. Contact with soil, and particularly gardening
and consumption of raw vegetables have been demonstrated to be significant risk factors for
toxoplasmosis in humans [69, 7, 70]. Contact with defecation sites is thus expected to result
in a high risk of infection, but, because contaminated sites represent a low proportion of the
The Life Cycle of Toxoplasma gondii in the Natural Environment 11
area, only a few humans are likely to be directly exposed. These persons include children
playing in sand pits, persons feeding the cats, gardeners, maintenance workers in these sites
and also dog owners who allow pets to roam in these sites and become indirectly exposed
through contact with dogs [71, 67, 68].
Overall, toxoplasmosis in urban areas should be characterized by heterogeneous dynamics,
with usually low levels of prevalence in cats, but locally high levels of soil contamination,
which may favour the environment-DH cycle.
4. Heterogeneity in the rural environment
Rural areas, and in particular agricultural landscapes, are suitable for T. gondii transmission,
due to the high densities of both DHs and IHs [72], and to the high level of predation.
However, this does not mean that rural areas are evenly infected. Spatial and temporal
variations have been detected at several scales. We first present the temporal dynamics to
identify mechanisms of heterogeneity that may also explain spatial variations.
4.1. Temporal dynamics
A temporal variability in the dynamics of T. gondii life cycle has been detected, both at the
year-to-year level and between seasons. It is first important to notice that temporal
variability is uneasy to study using serological data, because of the lifelong persistence of
antibodies. In long-lived species, temporal variations in the rate of appearance of new cases
(incidence) may be masked by the persistence of antibodies. The easiest ways to study
temporal dynamics of T. gondii should be to consider short-lived species, species where
antibody response does not persist lifelong, individual serological follow-up, or to consider
indicators of acute infection, i.e., type M immunoglobulins or oocyst excretion in cats.
Due to the difficulty to organize long-term surveys, year-to-year variations have been found
in a few populations only: in roe deer Capreolus capreolus in Spain [73] and in Sweden [74], in
red deer Cervus elaphus in Scotland [75], as well as in Canadian seals [76]. Tizard et al. [77]
performed the largest survey to our knowledge, with nearly 12,000 persons studied over 14
years. This survey revealed inter-annual 6-year cycles and showed that year-to-year
variations follow rainfall levels with a correlation coefficient as strong as 0.71. Accordingly,
a longitudinal survey of rural populations of domestic cats in France showed important
interannual variations in incidence among years, related to variations in the level of rainfall
[32]. In an urban site, seroprevalence in cats was highest during years with a hot and moist
weather or with a moderate and less moist weather [41]. The same trend was observed
during a long-term follow-up of two populations of roe deer, with maximal seroprevalence
under cold/dry, or cool/moist years [78].
The first explanation that has been proposed for the correlation between meteorological
conditions and T. gondii dynamics involves the survival of oocysts. The free stage of T. gondii
is subject to hard environmental conditions: in the terrestrial environment, its survival in
soil depends on temperature and moisture. Oocyst survival is maximal (> 200 days) for
Toxoplasmosis – Recent Advances
12
temperatures comprised between -6°C and +20 °C [79]. Above +20°C, dessication of oocysts
may occur [41, 80, 81], but moisture should prevent it [82, 83]. Under-6°C, the survival of
oocysts is reduced and their capacity to sporulate is lost [79], although one may hypothesize
that snow cover may protect them from cold. Meteorological variations are thus expected to
determine the survival of oocysts. Oocyst survival has also been demonstrated as one of the
parameters that most influence predictions given by a mathematical model [10]. However,
other factors may also vary with meteorological conditions and influence T. gondii life cycle.
In particular, the population dynamics of rodents is affected by climate-driven vegetation
growth [84]. Specifically, when winter is mild, survival is high and rodent populations
comprise many adult or old individuals, which are the age groups most often infected. Thus
the risk of encountering an infected prey is expected to increase after mild winters [32]. This
mechanism would contribute to the high transmission of T. gondii after mild winters, in
combination with high oocyst survival.
Meteorological conditions are also expected to act at the seasonal level. Oocyst survival
should be lowest during dry, hot summer periods, and during very cold winters. Moreover,
the population dynamics of hosts follows seasonal cycles: most births of rodents and cats
occur in spring and summer. However, since many kittens carry maternal derived
antibodies [41], the susceptible populations may increase in summer for rodents and in fall
for cats. We thus propose the following pattern (Figure 4): in summer, the low survival of
oocysts would lead to a low level of environmental contamination. However, the renewal of
the pool of susceptible rodents at the same period may boost T. gondii transmission. The
proportion of infected rodents would increase during summer and fall, thus increasing the
risk for cats to get infected. During fall and winter, kittens would have a maximal risk to get
infected and excrete oocysts. Finally, in spring, most cats born during the previous year and
highly exposed through hunting would have terminated their oocyst excretion thus the rate
of soil contamination would decrease. However, due to the survival of oocysts, the
prevalence in rodents would continue to rise, and would reach its maximal value at the
beginning of spring when reproduction starts again, giving birth to naïve rodents.
Following this scenario, the infection of domestic herbivores would increase at the end of
fall and in winter, when cats excrete oocysts, specifically within farm buildings [85], but
could continue up to the following spring, due to the high survival of oocysts. The risk for
infection of people would thus be maximal in winter when oocyst contamination and
herbivore infections are frequent, and may persist up to the following spring.
Because of the methodological difficulties presented above, many studies do not find any
seasonal pattern [47], and few data come in support of this hypothesis. Tizard et al.,
considering only high titres, found a clear decrease of human infections in fall [77]. This
decrease was interpreted as a consequence of the dry summer period, corresponding to low
oocyst survival. In Serbia, new infections occurred more often between October and April
than the rest of the year [86]. A seasonal pattern was also found in the proportion of cat
faeces presenting oocysts in Germany. Faeces collected between January and June (0.09%)
were significantly less often infected than those collected during the second part of the year,
between July and December (0.31%) [87]. These observations are concordant with the above
The Life Cycle of Toxoplasma gondii in the Natural Environment 13
Figure 4. Possible seasonal pattern of the transmission of T. gondii.
scenario, however, more detailed data and/or a theoretical approach are needed to fully
confirm the proposed pattern. Should this pattern be confirmed, the variability of risk with
time should be taken into account for management and prevention recommendations.
4.2. Spatial heterogeneity
Spatial heterogeneity of the infection in the rural environment has been demonstrated both
between regions and between areas within and around villages. Farm animals, being
restrained to agricultural areas, are particularly relevant to analyse spatial heterogeneities of
the circulation of T. gondii. However, studies concerning other species or humans may
provide useful information when the studied processes concern farms as well as
surrounding areas.
At the between-region scale, heterogeneity has essentially been shown to correlate with
climatic variations. The hypothesis of relationships between humidity, temperature and T.
gondii prevalence has been suggested in cattle in Serbia [88] and in sheep in Spain [89]:
regions with high humidity and moderate temperatures are considered as most favourable
for the sporulation and survival of oocysts. However, few data allowed authors to formally
analyse these relationships in farm animals. When comparing the incidence of
toxoplasmosis in rural cats living in three villages from distinct regions in France, Afonso et
al. found that the difference between the villages was explained by their level of rainfall [32].
Other surveys, considering wild-living species and humans, are in accordance with the
hypothesis of a climate-driven dynamics. Regional seroprevalences in woman in France
vary with temperature: they increase when mean temperature increases, but decrease when
the mean number of days below -5°C increases in the region [13]. In a national survey on the
wild boar Sus scrofa, the number of 10-day periods below -6°C was also found as a
determinant of T. gondii seroprevalence [90]. Still in the wild boar, in Corsica, prevalence
was highest at high altitude, where rainfalls are abundant and temperatures are low [91].
Overall, these and previous results (4.1) underline the importance of climate and
meteorological conditions in driving the temporal and spatial dynamics of T. gondii. These
Toxoplasmosis – Recent Advances
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environmental conditions probably also act at a very local scale, for example to affect soil
contamination in South-oriented versus North-oriented slopes, however this has not been
studied.
Within villages, the spatial organization of host populations leads to heterogeneities of T.
gondii between central villages, farm areas and fields. In particular, farm buildings and their
surroundings, which shelter both cats and IHs, constitute an important source of infection
for the surrounding areas. The spatial distribution of cases around a pig farm [72], and a
mathematical modelling approach [92] both confirmed that farms represent a source for the
whole rural environment. Farms also represent a source of infection for the surrounding
wild areas: in Corsica, the seroprevalence in wild boar increased with the density of farms in
the county [91].
Finally, the dynamics of T. gondii is also variable among farms. As expected, the presence of
cats often determines the risk of a farm being infected [93, 94], thus cat control is a key to the
control of toxoplasmosis in farms [95], as well as rodent control [96]. Other factors reported
to influence T. gondii prevalence are related to herd management: size and isolation of herd,
presence of a water point, type of feeding [97, 93]. These factors represent interesting control
points [96].
Overall, the rural environment, and in particular farms and their surroundings, are a major
source of infection, including for other areas. In particular, rural areas and farms are the gate
for T. gondii to circulate between the wild and domestic environments, thus their spatial
distribution, management and level of biosecurity are determinant in the possibility for T.
gondii to mix domestic and sylvatic cycles.
5. A sylvatic cycle for T. gondii?
Being able to infect many species, T. gondii is common in wildlife, both in DHs and IHs [2,
98, 46, 1]. The question of a sylvatic cycle, and of whether such a cycle would be separated
from the transmission in the domestic area, has been raised. A possible interpenetration
between domestic and wild cycles would have important consequences for the management
of T. gondii, since limiting the propagation of the parasite among domestic animals is only
feasible if there is no major wild source. The main tools available to investigate this question
are the analysis of genotypes that are present in both areas, and the understanding of
transmission pathways through epidemiological surveys.
However, the situation differs between temperate and tropical areas. Section 5.1 reviews the
factors associated with T. gondii infection in wild animals in temperate areas, and assesses
the risk of inter-transmission between domestic and wild cycles with its consequences in
terms of zoonotic hazard, animal health and population dynamics of highly susceptible wild
species. Section 5.2 shows that in Europe, and to a lesser extent in North America, strains
found in wildlife are similar to local strains found in domestic animals and the environment.
Finally, section 5.3 deals with the specific situation of tropical areas, where the separation
between domestic and wild cycles is clearer than in the temperate areas.
The Life Cycle of Toxoplasma gondii in the Natural Environment 15
5.1. The dynamics of T. gondii in wildlife in temperate climates
T. gondii infection in wildlife does not occur with the same probability in any species or
place. Wild-living species first have variable levels of susceptibility and exposure. Exposure
is largely determined by life history traits, especially feeding behaviour. In birds, where T.
gondii infection can be present at a high level in many wild birds without any clinical
impact, exposure to T. gondii is highest in carnivorous species [99]. High T. gondii
seroprevalence is also reported in large predator species as Lynx and the European wildcat
[100, 101] which is of epidemiological significance because infected felids shed oocysts in the
wild environment.
Among non-carnivorous species, the risk of infection is related to the risk of encountering
oocysts, thus to the level of contact with potentially contaminated soil. In rodents and
lagomorphs, home-range size, energy requirements and life expectancy are all expected to
be related to the probability to encounter T. gondii oocysts. As these traits are correlated to
body size [102, 103, 104, 46], large rodents species are more often found positive than small
ones [46]. Body size is thus a relevant indicator of prevalence in a given species, and also an
indicator of the risk for predators to get infected by preying on that species. Finally,
omnivores such as wild boar can acquire toxoplasmosis by incidentally ingesting infected
rodents and mainly by rooting and feeding from soil contaminated with oocysts excreted by
cats, as shown for other species with similar behaviour, e.g., poultry [105]. On the same way,
nutria Myocastor coypus is a terrestrial herbivorous but can also eat small insects that can
disseminate oocysts and mussels, which can accumulate oocysts [106, 107, 108]. Nutria and
wild boar are thus particularly exposed to infection by T. gondii [109, 110]. Besides being
potential source of T. gondii for scavengers, they constitute relevant species to monitor the
burden of oocysts in the wild environment and to study factors associated with the dynamic
of T. gondii infection.
The relationship between feeding behaviour and T. gondii infection may also act within
species: in a predator species for example, differences of feeding behaviour between genders
can lead to a T. gondii infection higher in one group compared to others. In an insular
population, male cats were more often infected than females, which may be related to the
fact that males are heavier and may feed on lagomorphs more often than females, which
prey mainly on small mammals [46].
Beside species feeding ecology, wild-living populations also have a spatially and temporally
structured risk. Like for rural populations (see 4), climatic and meteorological conditions are
significant factors explaining the spatio-temporal variations of T. gondii in wild populations
[111, 91, 90, 78, 112]. Another determinant factor is the proximity of agricultural activity: in
Corsican wild boar, seroprevalence was highest in counties with high farm densities [91].
The presence of domestic cats, including farm cats or feral cats essentially living on
predation, and wildcats and hybrid that may live close to rural areas [113], is probably an
important factor explaining the connection between the wild and domestic life-cycles of T.
gondii. Cats roaming into forest or rural landscape searching for preys may shed oocysts and
Toxoplasmosis – Recent Advances
16
contaminate the soil grazed by herbivorous or omnivorous IHs. The domestic-wild inter-
connection is thus expected to increase with the proportion of predatory cats in populations
and their densities. This connection is also expected to increase with landscape
fragmentation, which increases the surfaces where wild animals may come in contact with
cats habitat. Generally, the level of anthropization is a relevant proxy for the presence of
domestic cats and risk of toxoplasmosis in wild-living populations: in Sweden and Finland,
the north-South gradient found in ungulates and hares, respectively, has been interpreted as
the result of a declining presence of human settlements and cats in the North [74, 114, 115].
In Chile, the prevalence in American minks Neovison vison was highest at proximity of
human settlements [116]. Finally, when wild-living cats are present, they constitute a strong
determinant of T. gondii in wildlife: at the national level, T. gondii prevalence in French wild
boar is high in the area of presence of the European wildcat Felis silvestris [90]; in Alaska, the
prevalence of infection in herbivorous species reflects the distribution of lynx Felis canadensis
in the area [117]. Here it is important to underline that, in order to find relevant explanatory
spatial factors, these have to be measured at the appropriate scale. For example, farm
density may not be an appropriate estimator of the domestic cat population when
considered at the country level [90]. Similarly, as stated earlier (4.2.), oocyst survival
depends on the conditions experienced by oocysts in their microenvironment, whose range
can be lower than the home range of the studied host population, and also lower than the
scale at which meteorological data are usually obtained [90]. The difficulty to obtain data at
the right spatial scale may explain that some spatial patterns were not elucidated [118, 119].
On the other hand, the presence of cats or anthropized area is not the single way remote
areas may be contaminated. Within the natural environment, long-distance dispersal of T.
gondii is possible either as oocysts or cysts within IHs. An example of the first process is the
contamination of marine mammals along the Northern Pacific American coast. Genetic as
well as epidemiological studies suggest that southern sea otters Enhydra lutris nereis may be
contaminated following fecal contamination of soil by domestic and wild felids flowing
from land to sea through surface runoff, followed by the accumulation of oocysts in filter-
feeding marine invertebrates [120]. The dispersal of oocysts within the marine environment
is poorly known, but Massie and al. [121] recently proposed that migratory filter-feeding
fish, like northern anchovies Engraulis mordax and Pacific sardines Sardinops sagax, may
spread T. gondii throughout the ocean. On the other hand, the long-distance dispersal of T.
gondii within IHs may be illustrated in the case of the isolated archipelago of Svalbard,
where cats are absent. In this area, arctic foxes were found to carry T. gondii, whereas 751
grazing herbivores tested were all seronegative, indicating that contamination by oocysts is
uncommon in the area. Prestrud et al. [122, 123] proposed that T. gondii may have been
transported to arctic area by migratory birds.
All these processes act to spread T. gondii from domestic to wild, and within the wild
environment. A possible consequence of this large transmission is the threat on conservation
efforts of highly susceptible species [124]. In most species, T. gondii infection is generally
The Life Cycle of Toxoplasma gondii in the Natural Environment 17
unapparent, provoking only mild symptoms. However, a limited number of highly
susceptible species have been discovered, in which T gondii infection leads to frequent
clinical disease and mortality. Marsupials and New World monkeys, which have evolved
largely separately from cats, are among the most vulnerable species [2, 125]. Fatal
toxoplasmosis is also well-documented in hares (Lepus sp.), in northern Europe [114] and
Japan [126]. Hares that die of toxoplasmosis are in general in a normal nutritional state and
the disease is acute. The explanations for the failure to achieve equilibrium between the
host and parasite mainly focus on the host characteristics: a possible lack of cellular
immune response [127, 128], the negative impact of stress (food and diet disturbances,
exposure to cold, concurrent infections) on the immune response of this species, or even
the cumulative effect of immunosuppression induced by toxoplasmosis and stress [129]
have been proposed. A clinical expression of toxoplasmosis is also observed in a felid, the
Pallas' cats Otocolobus manul when raised in captivity [130, 131]. In fact, wild Pallas' cats
have minimal opportunity for exposure to T. gondii in their isolated natural habitat in
Central Asia and, typically, do not become infected with this parasite until being brought
into captivity. This could explain their extreme susceptibility to toxoplasmosis [132], which
could threaten conservation programs devoted to this species [133]. Although no specific
case has been documented in the wild, T. gondii may threaten local wild-living populations,
for example when new human settlements come in contact with isolated endangered
populations.
5.2. T. gondii strains in wildlife at temperate latitudes
Despite the presence of a sexual cycle, T.gondii maintains a highly clonal population
structure. The majority of isolates found belong to one of the three clonal lineages referred to
as type I, II and III [134]. Recently, a fourth clonal lineage, called haplogroup 12, has been
identified based on isolates from wildlife in the United States [135].
In Europe, the majority of isolates from wildlife contain type II strains, with a few type III
strains. From 26 T. gondii positive extracts from red fox Vulpes vulpes from Belgium
submitted to a genotyping analysis with 15 microsatellite markers [136], 25 were type II and
only one type III [137]. Similarly, using six loci microsatellite analysis, only type II strains
were observed in 46 French isolates including 21 from wild boar [138], 12 from roe deer, 9
from foxes, one from mouflon Ovis aries, red deer and mallard Anas platyrhynchos [139] and
one from tawny owl Strix aluco [140]. Using the same molecular technique, Jokelainen et al.
[141] also identified the clonal type II in 15 DNA extracts from hare (Lepus sp.) in Finland. In
a recent study in Central and in Eastern Germany, Hermann et al. [87] determined the
complete genotype has been determined for twelve samples tissues from red foxes, using
nine PCR-RFLP markers. In addition to T. gondii clonal type II apico II and apico I, type III
and T. gondii showing non-canonial allele pattern were observed. Interestingly, this study
showed evidence of a mixed infection, as well as infection with a T. gondii genotype that
may represent a recombination of T. gondii types II and III.
Toxoplasmosis – Recent Advances
18
Su et al. [142] developed a standardized restriction fragment length polymorphism (RFLP)
typing scheme based on nine mostly unlinked nuclear genomic loci and one apicoplast
marker. These markers enable one to distinguish the archetypal from atypical types. In
addition, mixed strains in samples can be easily detected by these markers. Mixed infection
of T. gondii strains in IHs has been previously reported [134, 143]. Detection of mixed
infection is of particular interest in epidemiological studies. For genetic exchange, the DH
must ingest different types of parasites from their prey at nearly the same time. The
frequency of mixed infections in IHs is a relevant indicator of the likelihood of the genetic
exchange to occur in the field. In Svalbard, a Norvegian arctic archipelago, 55 artic foxes
Vulpes lagopus were found infected with T. gondii: 27 (49.1%) harboured clonal type II (17/27
were apico I and 10/27 apico II) and four (7.3%) had clonal type III [123]. Strains from 22
foxes (40%) could not be fully genotyped, but two (3.6%) shared more than one allele at a
given locus. Again, the most prevalent genotype in this study was clonal type II (with apico
alleles I and II) with a few types III genotypes.
It is noteworthy that type II is also the dominant type in domestic mammals in Europe. For
instance, Dumètre et al. [144] showed by multilocus microsatellite analysis the
predominance of type II in sheep, which has also been previously described in humans. In
the same way, Halos et al. [145] analysed 433 hearts of sheep by using PCR-restriction
fragment length polymorphism and microsatellite markers on parasites isolated after
bioassay in mice. All 46 genotypes belonged to type II, except for one strain from the
Pyrenees mountains area, which belonged to genotype III, which is the first non-type II
genotype found in sheep in Europe [146], Denmark [147] and France [144]. This similarity
between strains found in wildlife and domestic species in Europe suggests that no clear
separation exists between the two cycles.
In North America, strains of T. gondii are more diverse. A recent study [148] analysed 169 T.
gondii isolates from various wildlife species including DHs and IHs, and revealed the large
dominance of a recently designated fourth clonal type, called type 12, followed by the type
II and III lineages. These three major lineages accounted for 85% of strains from wildlife in
North America [148]. The strains isolated from wildlife in North America are thus more
diverse, but may also be more different from strains found in the domestic environment
than in Europe. Although type 12 has been identified from pigs and sheep in the USA, it
may be more specifically found in wildlife [135]. The relative high diversity in T. gondii
genotypes isolated from wildlife samples compared to those from domestic animals raised
the question as to whether distinct gene pools exist for domestic and sylvatic hosts [149].
5.3. The wild environment in tropical areas
The wild environment in tropical areas is still characterized by high fauna diversity, and
large areas preserved from influence of humans and of domesticated animals, including
cats. Studies on T. gondii seroprevalence conducted on tropical wild animals, mainly in
South America, show the wide circulation of T. gondii in the wild environment of these
The Life Cycle of Toxoplasma gondii in the Natural Environment 19
countries. As in temperate climate [150], the prevalence of T. gondii infection was higher in
carnivorous or carrion-eaters, or those that accidentally consume oocysts while foraging for
food on the ground than in arboreal animals [151]. It was also remarkably high in aquatic
mammals such as free-living Amazon River dolphins Inia geoffrensis [152]. Remote human
population living in wild environment may also exhibit high seroprevalence level for T.
gondii infection, for example 60.4% in Amerindian tribes [153] or 38.9% in Pygmies from
Central Africa [154]. As domestic cats are generally absent from this environment, wild
felids are the main source of water and soil contamination. Thirty-nine species of felids have
been described, of which 20 live in humid tropical areas [155, 156]. The capacity of oocyst
excretion has been demonstrated in captivity, and high seroprevalences were found on free-
living felids [157]. In captive Neotropical felids from Southern Brazil, wild-caught felids
were three-times more likely to be infected when compared to zoo-born animals [158]. The
different species of wild felids varied in home range and resource requirements, but they
generally have larger hunting areas and dietary intake than domestic cats, especially the
largest ones [159]. This could result in a high opportunity to ingest T. gondii infected preys.
So, despite the fact that the ecology of T. gondii in the wild tropical environment has been
poorly studied, the different behaviour of wild felids compared to that of domestic cats and
the number of possible IHs suggest a complex ecology of this parasite in this environment
leading to a high genetic diversity [160].
This high genetic diversity in tropical wild-life in connection with a sylvatic life cycle has
been firstly evoked in French Guiana where severe cases of human toxoplasmosis were
detected after eating Amazonian undercooked game or drinking untreated river water [161,
162, 163]. These cases were due to highly atypical strains, all with unique genotype, as
determined by microsatellite analysis [164]. The difference between these strains acquired
from the Amazonian environment and strains from the anthropized environment of French
Guiana was further documented by strain sampling in animals from the different
compartments [165].
Compared to the strains of the anthropized environment, the “wild” strains from the
Amazonian rainforest in the Guianas exhibited a remarkably high genetic diversity [162,
164, 165]. Whereas the majority of strains from the adjacent anthropized environment are
clustered into a few widespread lineages, the “wild” population of strains does not exhibit
any clear genetic clustering/structure nor any linkage disequilibrium, supporting the
hypothesis of an important circulation and mixing in this environment. This could be
connected to the high level of biodiversity in Amazonian neotropical rainforest. This
biodiversity concerns the different protagonists of T. gondii life cycle (DH, IH and
environment). This part of the world may be considered as one of the most important
hotspot of diversity with at least 183 mammal species, including 8 of thirty nine known wild
felid species, and 718 bird species in French Guiana [165]. The corresponding high level of
diversity among T. gondii strains may reflect the “natural” population structure of this
parasite (before the time of domestication of cats and development of farming) within the
Toxoplasmosis – Recent Advances
20
true complexity of less disturbed ecosystems. The relative richness of potential hosts that
exists within the tropics may have resulted in a correspondingly more diverse range of
genotypes of the parasite that can co-exist in such an environment. Under this hypothesis, T.
gondii would have developed a plurality of alleles to increase its colonization potential [160,
162]. In addition, the larger home ranges of wild felids compared to domestic cats can also
strongly influence hybridization patterns and gene flow of the parasite and thus the genetic
structure of pathogen populations. The high prevalence in IHs, added to wild felid ecology
(diet and home range), could suggest that DHs are more frequently infected by multiple T.
gondii genotypes, which then cross and recombine before transmission to a new IH. The
possibility of reinfection by different strains is known for humans [166]. It has never been
explored for felids, but may be hypothesized as another source of increasing diversity.
Most tropical countries are also characterized by an ongoing anthropization with
development of farming and settlement in deforested areas. At the confluence between the
two environments, wild animals may penetrate in anthropized areas and domestic animals
come in contact with the wild through wild game, soil or running water. The increasing
pressure of anthropization reduces the hunting area of wild carnivores, including felids and
favours their penetration in domestic area. The predatory activity of wild felines or stray
cats around these disturbed environments (consumption of chickens, dogs, cats…) would
ensure gene flow between the two populations of strains. The consequences of this
interpenetration in terms of T. gondii genotypes are diverse: (i) detection of T. gondii strains
with “hybrid” genotypes between the “wild” population and the anthropized population
reflecting genetic exchanges, (ii) strains from the wild environment found in domestic
animals, such as stray dogs, or (iii), on the opposite, strains from the anthropized
environment found in wild animals [165]. In parallel, the influence of human activities with
urbanization, fragmentation of landscape, deforested areas, farming, domestication of cats
and other animals, modifies T. gondii ecology reducing the number of ecological niches. This
process favours an impoverishment of T. gondii genetic diversity with the selection of a few
strains well adapted to a small number of domestic species [167, 168]. Transportation of
these strains through large distances by human trade exchange and transportation of
animals lead to introduction of domestic strains in the wild environment and occasionally to
expansion of clonal lineages. In tropical countries, this is evidenced by the so-called
Caribbean genotypes found in the anthropized areas of French Guiana and in several
Caribbean Islands, or in Africa, where the same African lineages were found in different
countries [169, 170, 171].
Finally, the dynamics of T. gondii in wildlife and its interaction with domestic areas show a
contrasted pattern. In most European countries, due to the large anthropization, any wild-
living individual lives relatively close to domestic areas. Farming and cat domestication
occurred long time ago. Farms constitute the reservoir of infection, from which a few
genotypes adapted to farm species irradiate in the surrounding environment [72]. This
could explain the widespread occurrence of only a few well adapted clonal lineages (types II
The Life Cycle of Toxoplasma gondii in the Natural Environment 21
and III) even in wild animals. In other temperate or cold countries, such as the U.S.A. or
Canada where large territories are non-anthropized, the genotypic diversity of T. gondii in
the wild animals is present [148, 149, 172]. The diversity is maximal in tropical areas, due to
high host diversity and large non-anthropized areas. Thus the risk of transmission of
toxoplasmosis from wildlife has not the same consequences everywhere. In tropical areas,
specific “wild” strains may be transmitted, thus the transmission risk is relatively easy to
characterize through strain genotyping, while in Europe, a case of infection acquired from
wildlife would pass unnoticed due to the similarity of strains. The risk of infection from
wildlife may be analyzed through genotyping strains in tropical areas, but through
epidemiological surveys in Europe.
6. Conclusion: consequences for the management of zoonotic
transmission
Like other IHs, humans can be infected either by cysts containing bradyzoits, or by oocysts
of T. gondii. Tissue cysts are responsible for meat-borne infection (pork, lamb, beef or
poultry are possible source of contamination), while sporulated oocysts lead to infection by
ingesting particles of soil (after gardening for example) or by consuming unwashed raw
fruits or vegetables, or untreated water [2, 145, 173, 174, 175]. However, the crucial question
of the relative part of risk related to bradyzoits versus oocysts remains open. Different
approaches have been used to estimate the relative importance of sources of contamination,
using risk-factor analyses or estimation of the fraction of attributable risk, either in the
general population (chronic infection) or in cases of seroconversion in pregnant women.
These studies clearly identified the ingestion of undercooked meat as a risk factor [7, 13, 173,
176]. However, this result is probably partly due to this risk being easier to characterize than
the risk due to oocysts. Another way to get an idea of the relative part of risk related to cysts
or oocysts is to undertake a quantitative assessment of the risk of toxoplasmosis [177].
Recently, in the Netherlands, Opsteegh et al. performed a quantitative microbial risk
assessment (QMRA) for meat-borne toxoplasmosis, which predicted high numbers of
infections per year. The study also demonstrated that, even with a low prevalence of
infection in cattle, consumption of beef constitutes an important source of infection [178].
However, the risk assessment remains limited by the lack of detailed information on which
fraction of meat is more contaminated in carcass: although seroprevalences are available for
farm animals from many countries [2], the correlation between seropositivity and detection
of parasites in meat is weak. In terms of veterinary medicine, there is no surveillance system
for animal toxoplasmosis and only cases of abortions (due to T. gondii or other causes) have
to be declared. The meat-borne risk analysis is also limited by the low level of information
on the food cooking practices, and on the contamination of species consumed less often,
such as game [90, 91, 78].
Up to now, the risk analyses essentially used information on, and produced estimates about,
meat-borne toxoplasmosis. These studies permitted to identify control points for the
Toxoplasmosis – Recent Advances
22
management of meat-producing animals. For example, in intensively managed swine farms,
modern biosecure management practices have resulted in reduced levels of infection in
swine raised in confinement [96, 179, 180]. In organic livestock production systems, farm-
management factors including feeding are thought to play an important role in the on-farm
prevalence of T. gondii [181]. To limit T. gondii infection in such farms, recommended
practices include exclusion of cats or other wildlife, strict rodent control and restriction of
human entry in pig barns [182]. These measures could be effective in other species to reduce
the level of contamination of meat. On the contrary, organic pork meat may pose a specific
risk of transmitting T. gondii to humans [183]. However, due to the capacity of dissemination
of T. gondii, the objective of a completely T. gondii-free meat seems difficult, but feasible
using pre-harvest measures for prevention of T. gondii infection [184].
On the other hand, working to reduce the level of infection in meat does not act on the risk
of toxoplasmosis due to direct contact with oocysts, which stays largely unknown and
unmanaged. Limiting the level of contamination in meat may even result in the increase of
the relative risk due to oocysts. The importance of oocysts in the overall contamination rate
remains difficult to assess, due to the lack of information on the level of environmental
contamination and to the difficulty to characterize the level of contact of people with
contaminated areas. In this framework, a better knowledge of the life cycle of T. gondii in its
natural environment should help to characterize the risk due to oocysts. For example, the
estimates provided in Table 1 give an order of magnitude of the expected differences
between environments. Moreover, two recent methodological advances should improve our
knowledge of environmental contamination. First, new methods to detect oocysts in soil
[185] and water [186, 187, 188] have been proposed, based on molecular detection or
immunocapture. Being highly sensitive, these methods should allow researchers to better
characterize areas and periods at risk of contamination. A few studies have already
measured the level of soil and water contamination [50, 68, 189]. These studies confirmed
that the risk in urban areas is spatially structured at the very local scale, and they should
help to identify areas most contaminated in other environments. The second useful tool that
should bring relevant information is the development of methods to detect antibodies
specifically linked to infection by oocysts [190]. This test, based on western blot assay
detecting for IgG positive serums antibodies to sporozoites, allowed the authors to
determine the proportion of cases that had contacts with oocysts in Chile, both in humans
[191] and in swine [192]. In North America, a survey using this method shows that a high
proportion of mothers of congenitally infected infants had primary infection with oocysts
[193].
These new analytical tools should help to identify the origin of contamination, and thus
solve several fundamental and practical questions regarding T. gondii life cycle. For
example, estimating the frequency of infection from oocysts in cats of urban and rural area
should help to estimate the part of the DH-environment life cycle in different environments.
In people, these tools should help to assess if the relative role of oocyst and meat-born
infection varies according to the area (urban versus rural populations for example). In such
The Life Cycle of Toxoplasma gondii in the Natural Environment 23
case, prevention measures should focus on specific aspects depending on the exposure of
people. These elements should help to reduce the burden of toxoplasmosis in human and
animal populations.
Author details
Emmanuelle Gilot-Fromont1,2,*, Maud Lélu3, Marie-Laure Dardé4, Céline Richomme5,
Dominique Aubert6, Eve Afonso7, Aurélien Mercier4, Cécile Gotteland1,6, Isabelle Villena6
1UMR CNRS 5558 Laboratoire de Biométrie et Biologie Evolutive, Université Lyon 1, Villeurbanne,
France.
2VetAgro-Sup Campus Vétérinaire, Université de Lyon, Marcy l’Etoile, France,
3NIMBioS, University of Tennessee, Knoxville, Tennessee, USA,
4INSERM UMR1094, Tropical Neuroepidemiology, School of Medicine, Institute of
Neuroepidemiology and Tropical Neurology, CNRS FR 3503 GEIST, University of Limoges,
Limoges, France,
5ANSES, Nancy laboratory for rabies and wildlife, Technopole agricole et vétérinaire, Malzéville,
France,
6Laboratoire de Parasitologie-Mycologie, EA 3800, UFR de Médecine, SFR Cap Santé, FED 4231,
University of Reims Champagne-Ardenne, Reims, France,
7Department Chrono-environnement, UMR CNRS 6249 USC INRA, University of Franche-Comté,
Besançon, France
Acknowledgement
The authors thank Aurélien Dumètre, René Ecochard, Michel Langlais, Dominique Pontier,
Philippe Thulliez and Stéphane Romand for their help in elaborating the 10-year research
period that produced part of the results presented here. This project has been supported by
the Agence Française de Sécurité Sanitaire de L’Environnement et du Travail (AFSSET) and
by the Agence De l’Environnement et de la Maitrise de l’Energie (ADEME), with additional
grants from Grünenthal France Laboratory (EA), Institut National de la Recherche
Agronomique (INRA, CR), Région Champagne-Ardenne (EA, ML and CG), Département
des Ardennes (ML), Communauté de Communes de l'Argonne Ardennaise (ML) and the
National Institute for Mathematical and Biological Synthesis (NIMBioS, sponsored by the
National Science Foundation, the U.S. Department of Homeland Security, and the U.S.
Department of Agriculture, ML).
7. References
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* Corresponding Author
Toxoplasmosis – Recent Advances
24
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... T. gondii can be found anywhere in the world and in humans infection can cause life-threatening encephalitis in immunocompromised individuals such as HIV/AIDS patients or organ transplant recipients (McFarland et al., 2016). Infection acquired during pregnancy may spread into the foetus and cause severe damage to foetal development (Gilot-Fromont et al., 2012;Blader et al., 2015). The T. gondii life cycle starts in felids usually through the consumption of infected prey containing tissue cysts. ...
... Tachyzoites (tachos = fast) and bradyzoites (brady = slow) are rapidly and slowly growing stages of T. gondii, respectively (Dubey, 2002(Dubey, , 2006(Dubey, , 2010. Domestic cats are infected through consuming either sporulated oocysts or intermediate hosts containing tissue cysts (Gilot-Fromont et al., 2012). To be infective, an unsporulated oocyst is converted into a sporulated one within 1-5 days (Black and Boothroyd, 2000;Gilot-Fromont et al., 2012). ...
... Domestic cats are infected through consuming either sporulated oocysts or intermediate hosts containing tissue cysts (Gilot-Fromont et al., 2012). To be infective, an unsporulated oocyst is converted into a sporulated one within 1-5 days (Black and Boothroyd, 2000;Gilot-Fromont et al., 2012). T. gondii undergoes asexual replication in all warm-blooded vertebrates or in intermediate hosts (Ferguson, 2009). ...
... T. gondii has a complex lifecycle, involving sexual replication in felids (cats) as the definitive host and asexual propagation in humans and other mammals as intermediate hosts (Gilot-Fromont et al., 2012). Felids excrete millions of oocysts in the environment. ...
... Felids excrete millions of oocysts in the environment. The sporulation, survival, and infectivity of excreted oocysts is dependent on environmental and climatic conditions (Gilot-Fromont et al., 2012;Meerburg and Kijlstra, 2009). A recent systematic review and meta-analysis indicated that almost 16% of public places across the world are contaminated with Toxoplasma oocysts (Maleki et al., 2020). ...
... In recent years, there is a growing body of literature suggesting that the environmental-related risk factors and geo-climatic parameters are significantly associated with the distribution of Toxoplasma infection (Gilot-Fromont et al., 2012;Lélu et al., 2012;Rostami et al., 2019;Shapiro et al., 2019). However, to date, there is only one meta-analysis that assessed the relationship between geo-climatic parameters and Toxoplasma infection in pregnant women, and it only considered the articles up to November 30, 2018 (Rostami et al., 2019). ...
Article
In this study, we evaluated the effects of geo-climatic parameters and other potential risk factors on the prevalence of chronic toxoplasmosis (CT) in pregnant women. We searched PubMed/MEDLINE, Web of Science, EMBASE, Scopus, and SciELO databases for seroepidemiological studies published between January 1988, and February 2021. We performed meta-analysis and meta-regression by using a random effect model to synthesize data. A total of 360 eligible datasets, including 1,289,605 pregnant women from 94 countries, were included in this study. The highest and lowest prevalence rates were estimated for latitudes of 0-10° (49.4%) and ≥50° (26.8%); and for the longitude of 80–90° (44.2%) and 110-120° (7.8%), respectively. Concerning climatic parameters, the highest and lowest prevalence rates were estimated in regions with the mean relative humidities of >80% (46.6%) and <40% (27.0); annual precipitation between 1000-1500 mm (39.2%) and 250-500 mm (26.8%); and mean annual temperature of 20-30 °C (36.5%), and <7 °C (24.9%), respectively. Meta-regression analyses indicated significant increasing trends in prevalence of CT in pregnant women with decrease in geographical latitude (coefficient, = -0.0035), and geographical longitudes (C = -0.0017). While it was positively associated (P<0.01) with the mean environmental temperature (C = 0.0047), annual precipitation (C = 0.000064), and mean relative humidity (C = 0.002). Our results highlighted the various effects of environmental parameters on the prevalence of CT in different regions. Therefore different regions in the world may benefit from different types of interventions, and novel preventive measures in a region should be developed according to local climate, agricultural activities and people culture.
... Toxoplasma gondii is an obligate intra-cellular protozoan parasite that can infect most vertebrate animals and causes a disease called Toxoplasmosis (1). It was originally identified in a North African rodent called the gundi, from which it derives its specific name (2,3). ...
... It was originally identified in a North African rodent called the gundi, from which it derives its specific name (2,3). Humans can become infected by ingestion of oocysts released from cat feces, consumption of undercooked and raw meat, or drinking of unpasteurized milk containing T. gondii tissue cysts (1,4). Transplacental congenital transmission of tachyzoites, blood transfusion, and organ transplantation were very rarely reported (5,6). ...
Article
Full-text available
Introduction: The majority of human infections with Toxoplasma gondii produce no symptoms, but in congenitally infected children can cause devastating effects including blindness, brain damage, or miscarriage. Transmission to the fetus occurs predominantly in women who acquire their primary infection during gestation. The study aimed to assess the seroprevalence of toxoplasmosis among pregnant women attending antenatal care (ANC) in different areas of Asmara, Eritrea, and to identify possible risk factors associated with toxoplasmosis among pregnant women attending the ANC centers. Methods: In this cross-sectional laboratory-based study, the data were collected from 210 pregnant women in four health facilities. Voluntary sampling technique and a structured questionnaire were used to collect the associated data and socio-demographic information. Cobas e411 Analyzer was used to test the blood serum for immunoglobulin G (IgG) and Immunoglobulin M (IgM) antibodies. Epi-Info version 7.0 was used for data entry and SPSS version 20.0 was used for data analysis. Results: Of the 210 samples, 112 (53.6%) samples were seropositive and 97 (46.4%) samples were seronegative for T. gondii specific IgG antibody. Furthermore, 2.9% (6) of the samples were seropositive and 97.1% (203) of the samples were seronegative for T. gondii-specific IgM antibodies. Conclusion: The seroprevalence was considerably high, 53.6% for IgG antibody and 2.9% for IgM antibody, which require attention in order to implement preventive control measures, screening tests, and health education.
... This could also occur in mixed T. gondii infections in hyperendemic regions, where some strains may be resistant to some chemotherapeutics and are the cases that do not respond to the current treatment against the parasite. In addition, the two sampled cats were feral, and these animals obtained their whole diet from hunting small mammals and birds; if the cats consume prey infected with different genotypes within several days, it is possible that more than three genotypes could be found circulating in their blood because tachyzoites can be found up to 10 days after oral infection [22][23][24]. ...
Article
Full-text available
Background Currently, more than 300 genotypes of Toxoplasma gondii (T. gondii) have been described throughout the world, demonstrating its wide genetic diversity. The SAG3 locus is one of the genes included in the genotyping panel of this parasite. It is associated with its virulence since it participates during the invasion process of the host cells. Therefore, cloning, sequencing, and bioinformatic analysis were used to deepen the understanding of the SAG3 locus genetic diversity of T. gondii in blood samples from feral cats. Results Six different SAG3 sequences were detected, five of which were detected in one feline. Three sequences were first reported here; one of them was an intragenic recombinant. In the cladogram, four out of ten SAG3 sequences did not share nodes with others reported worldwide. Conclusions Cloning and sequencing of samples with more than one restriction pattern by PCR-RFLP were very helpful tools to demonstrate the presence of more than three genotypes of T. gondii in the blood of feral cats from southeastern Mexico. This suggests a potential mixed infection of multiple T. gondii strains and high genetic diversity of the parasites in felines in this tropical region of Mexico.
... Our second set of hypotheses considered climatic factors since temperature and precipitation affect oocyst survival and transport in the environment and domestic cat abundance and free-roaming activity [26]. Extreme temperatures can reduce oocyst survival [27], while heavy precipitation facilitates oocyst transport in terrestrial and aquatic ecosystems [28]. ...
Article
Full-text available
Macroecological approaches can provide valuable insight into the epidemiology of globally distributed, multi-host pathogens. Toxoplasma gondii is a zoonotic protozoan that infects any warm-blooded animal, including humans, in almost every ecosystem worldwide. There is substantial geographical variation in T. gondii prevalence in wildlife populations and the mechanisms driving this variation are poorly understood. We implemented Bayesian phylogenetic mixed models to determine the association between species’ ecology, phylogeny and climatic and anthropogenic factors on T. gondii prevalence. Toxoplasma gondii prevalence data were compiled for free-ranging wild mammal species from 202 published studies, encompassing 45 079 individuals from 54 taxonomic families and 238 species.We found that T. gondii prevalence was positively associated with human population density and warmer temperatures at the sampling location. Terrestrial species had a lower overall prevalence, but there were no consistent patterns between trophic level and prevalence. The relationship between human density and T. gondii prevalence is probably mediated by higher domestic cat abundance and landscape degradation leading to increased environmental oocyst contamination. Landscape restoration and limiting freeroaming in domestic cats could synergistically increase the resiliency of wildlife populations and reduce wildlife and human infection risks from one of the world’s most common parasitic infections.
... Cats are the definitive hosts for T. gondii. Rodents serve as reservoir hosts for various pathogens and have been shown to play a chief role in the transmission of several infectious diseases to animals and humans [4,5]. Rats as herbivores are susceptible to T. gondii infection due to the consumption of food/water contaminated with oocysts present in environments [4,6]. ...
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... An indirect approach for determining T. gondii distribution in the environment is accomplished through detecting the parasite prevalence in intermediate hosts. Rodents and birds play an important role as intermediate hosts in the T. gondii life cycle because they are the main source of infection for several feline definitive hosts (Love et al., 2016;Gilot-Fromont et al., 2012). Rodents and birds also serve as a food source for predatory birds, such as raptors. ...
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Chapter 3 defines urban ecosystems and elaborates the specifics of these compared to other ecosystems, especially agricultural or forest systems, in terms of their properties and basic functionality. The abiotic bases and properties of urban ecosystems are described in detail. Different ways of delimiting urban ecosystems including their advantages and disadvantages are also discussed. In addition, Chapter 3 introduces and critically evaluates different concepts of urban ecosystems. Information boxes inform about current topics, methods and case studies.
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