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Background:
Systematic Review

Anti-Toxoplasma gondii Antibodies in European Residents: A Systematic Review and Meta-Analysis of Studies Published between 2000 and 2020

by
Rafael Calero-Bernal
1,*,
Solange María Gennari
2,3,
Santiago Cano
4,
Martha Ynés Salas-Fajardo
1,
Arantxa Ríos
1,
Gema Álvarez-García
1 and
Luis Miguel Ortega-Mora
1
1
SALUVET, Animal Health Department, Complutense University of Madrid, 28040 Madrid, Spain
2
PhD Program in One Health, Faculty of Veterinary Medicine, University of Santo Amaro, São Paulo 04829-300, SP, Brazil
3
Faculty of Veterinary Medicine, University of São Paulo, São Paulo 05508-270, SP, Brazil
4
Computing Services, Research Support Center, Complutense University of Madrid, 28040 Madrid, Spain
*
Author to whom correspondence should be addressed.
Pathogens 2023, 12(12), 1430; https://doi.org/10.3390/pathogens12121430
Submission received: 19 October 2023 / Revised: 24 November 2023 / Accepted: 7 December 2023 / Published: 8 December 2023
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Abstract

:
Toxoplasmosis has a major impact on animal and public health. Information regarding the seroprevalence of human Toxoplasma gondii infections from a European perspective has not yet been compiled to date. Thus, the present review summarized available resident data from the period 2000–2020. The overall seroprevalence of anti-T. gondii IgG was 32.1%, with great variability between countries (n = 30). The subgroup analysis identified different pooled prevalence data depending on the geographic area (p < 0.0001), target population (p = 0.0147), and serological diagnosis assays used (p = 0.0059). A high heterogeneity (I2 = 100%, p < 0.001; Q = 3.5e+05, d.f. = 135, p < 0.001) and degree of publication bias (Egger’s test = 6.14, p < 0.001) were observed among the 134 studies considered. The occurrence of anti-T. gondii IgM, which was reported in 64.7% of studies, reached a pooled seroprevalence of 0.6%. In addition, among the eight main risk factors identified, “contact with soil”, “consumption of undercooked beef”, and “intake of unwashed vegetables” were the most significantly associated with infections. The fact that one-third of the European population has been exposed to T. gondii justifies extra efforts to harmonize surveillance systems and develop additional risk-factor analyses based on detailed source attribution assessment.

1. Introduction

Toxoplasma gondii is an apicomplexan intracellular parasite capable of infecting almost all homoeothermic animals, including humans [1]. Toxoplasma gondii is characteristically opportunistic, and may be especially harmful in immunocompromised patients (HIV-positive, solid organ transplant recipients, etc.), but also when primary infections occur during pregnancy; congenital infections may lead to important reproductive disorders from abortions, fetal malformations, or diverse mental-retardation sequelae in children. A global disease burden estimation study [2] identified an association between the occurrence of latent toxoplasmosis and specific disease burden in 88 countries, and indeed such correlations between the presence of anti-Toxoplasma antibodies and age-standardized disability adjusted life years (DALY) explained 23% of the variability in disease burden in 29 European countries.
Comprehensive literature reviews of the status of T. gondii infections (a major zoonosis) in domestic and wild animals in Europe have been carried out [3,4]; nevertheless, regarding human populations, only one paper [5] reviewed the epidemiological situation focused on the Balkan countries (southeast Europe), and therefore no studies have been carried out from a pan-European perspective to date. Two studies analyzed the current surveillance schemes set up in Austria, France, and the USA, and highlighted the need to harmonize diagnosis and monitoring systems in most countries [6,7].
Despite the incidence of congenital toxoplasmosis in Europe (5.8 cases per 100,000 live births), which is ranked among the top causes of disease burden in EU/EEA when evaluating the disability-adjusted life years parameter [8,9], well-structured investigations concluded that most T. gondii-infections in the EU had a food-borne origin [10]. In this regard, a pioneer multicenter case–control study aiming at the identification of sources of Toxoplasma-acute infections in pregnant women in Europe [11] suggested eating undercooked lamb, beef, or game meat, contact with soil, and traveling outside Europe, USA, and Canada as the major risk factors. However, remarkably, contact with cats was not identified as a risk factor. In agreement, a later meta-analysis that was focused on worldwide consumption habits [12] identified the intake of raw/undercooked beef and lamb meat as risk factors significantly associated with acute T. gondii infections in humans. In spite of this, the authors exposed the limitations due to the low number of case–control studies available. Recently, a case–control study identified consumption of meat of large game animals and poor hand hygiene as key risk factors for acute toxoplasmosis in the Netherlands [13]. The complex epidemiology of T. gondii is responsible for the high number of risk factors of infection reported worldwide (reviewed in [14]). Currently, some habits and trends may have changed in the European population. In recent years, an increase in T. gondii infection cases has been clearly associated with fresh vegetable consumption [15], and it has been demonstrated that the environmental route of infection may involve a wide set of potential sources [16]. Accordingly, new studies approaching the source attribution of T. gondii infections have resulted in major interest [17].
As commented above, no review paper focused on seroprevalence data on European human populations has been carried out yet; therefore, the present article aimed to systematically review and carry out a further meta-analysis of the available literature regarding two important aspects in observational studies published from 2000 to 2020: seroprevalence (IgG and IgM) data and the most suitable risk factors involved in T. gondii infections in European residents.

2. Materials and Methods

The present study was carried out according to the PRISMA guidelines (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) [18], and the PRISMA checklist is available in Supplementary Table S1. The performance workflow followed in the present study is shown in Figure 1.
Literature published between January 2000 and December 2020 was searched in electronic databases (PubMed, Science Direct, Scopus, WoS and SCIelo) using medical subject headings (MeSH) terms (Toxoplasma gondii, toxoplasmosis, seroprevalence, human, Europe); selection (eligibility criteria: serosurveys [excluding review papers; case–control studies were only considered for the risk factors study/analyses], years 2000 to 2020, continental Europe, any language); and further critical review and a meta-analysis were carried out as previously proposed [19]. Initially, abstracts were revised for study screening and further data extraction; the whole process was carried out by two investigators. Additional references cited in the bibliography of the evaluated papers were considered eligible. Papers in languages other than English (to note: Croatian, French, German, Icelandic, Italian, Polish, Portuguese, Serbian, Spanish, and Russian) were taken into consideration.
From each eligible study dealing with anti-T. gondii IgG and IgM data or risk factors analysis, detailed information on study area, year/data of sampling, target population, diagnostic method, sample size, and number of positive samples was collected. In addition, data on significant risk factor conditions (odds ratio, relative risk, and significance) were gathered in those specific studies (Supplementary Table S2). Regarding data analysis, for the evaluation of pooled estimates (detection rates reported in each study), a restricted maximum likelihood method with a random effects model was used [20]. Study bias and heterogeneity at the study level were calculated using Egger’s test, and Cochran’s Q test and inverse variance index (I2), respectively [20,21,22]. Alpha was set at 0.05.
Statistical analyses were performed using STATA 15.0 software (StataCorp, Bryan, TX, USA).

3. Results

3.1. Seroprevalence of Anti-T. gondii IgG in European Residents

A total of 136 published studies on T. gondii IgG seroprevalence in humans in Europe, published between 2000 and 2020, with 30 countries represented, were eligible and included in this meta-analysis (Table 1). Europe was divided into 4 regions: North, with 7 countries (Estonia, Finland, Iceland, Ireland, Norway, Sweden, and United Kingdom) and 51 published studies; West, with 6 countries (Austria, Belgium, France, Germany, Netherlands, and Switzerland) and 47 studies; East, with 6 countries (Czech Republic, Hungary, Poland, Romania, Russia, and Slovakia) and 18 publications; and finally South, with 11 countries (Albania, Bosnia and Herzegovina, Croatia, Cyprus, Greece, Italy, North Macedonia, Portugal, Serbia, Slovenia, and Spain) and 20 studies. For the analysis of IgG seroprevalence, the samples were obtained from the following: general population (n = 38 studies), pregnant women or women of childbearing age (n = 58), and others (n = 47), and the diagnostic methods that were used were based on commercial tests (n = 101 studies), in-house tests (n = 15), and a combination of both (n = 8) (Table 2).
Figure 2A illustrates the pooled T. gondii IgG seroprevalence values by European country. The overall IgG seroprevalence was 32.1% (95% CI 29.0–35.2), with values of 20.1% (95% CI 16.8–23.5), 38.5% (95% CI 29.7–47.2), 39.7% (95% CI 32.1–47.2), and 27.5% (95% CI 24.3–30.7) for North, West, East, and South regions, respectively, and statistically significant differences (Student’s t-test) were observed between areas (p < 0.05) except between the West and East areas (p < 0.8384).
Regarding target populations, the IgG seroprevalences were 38.6% (95% CI 33.7–43.6) for the general population (e.g., healthy people of different ages), 28.3% (95% CI 24.2–32.4) for pregnant women or women of childbearing age, and 31.1% (95% CI 29.0–33.1) for other groups of the population considered to be people at higher risk (e.g., health care workers, abattoir workers, farmers, hospital patients, etc.). Statistically significant differences were observed for seroprevalence in the general population compared to that of pregnant women/women of childbearing age (p = 0.011).
The frequencies obtained of T. gondii IgG antibodies for the type of diagnostic method used were 30.2% (95% CI 28.1–32.3), 40.1% (95% CI 35.4–44.8), and 43.2% (95% CI 35.4–51.0) for commercial, in-house, and a combination of both, respectively, and a statistically significant difference (p = 0.011) was observed when commercial and in-house methods were compared. Supplementary Figures S1 and S2 present the forest plot of the seroprevalence of IgG antibodies by country and funnel plots of IgG seroprevalence by the variables analyzed (region, type of population, and analytical methods), respectively. A high heterogeneity (I2 = 100%, p < 0.001; Q = 3.5 × 105 (d.f. = 135), p < 0.001) and degree of publication bias (Egger’s test = 6.14, p < 0.001) were observed among the 134 studies considered.

3.2. Seroprevalence of Anti-T. gondii IgM in European Residents

Figure 2B illustrates the anti-T. gondii IgM results per European country, and Table 3 summarizes the characteristics of the 88 eligible studies. The pooled T. gondii IgM seroprevalence was 0.6% (95% CI 0.5–0.6), with values of 0.1% (95% CI 0.0–0.1), 0.2% (95% CI 0.1–0.3), 1.5% (95% CI 1.3–1.8), and 1.1% (95% CI 1.0–1.3) for the North, West, East, and South regions, respectively. Statistically significant differences (Student’s t-test) were observed between all areas (p < 0.001) except between the North and West (p = 0.073). A high heterogeneity (I2 = 99.1%, p < 0.001; Q = 6697.26 (d.f. = 66), p < 0.001) and degree of publication bias (Egger’s test = 6.52, p < 0.001) were observed among the 67 studies considered for statistical analyses.
Most of the studies (65.9%; 58/88) focused on the detection of IgM antibodies in pregnant women or newborn children as the main target populations; as expected, different frequencies of IgM detection were observed: 0.1% (95% CI 0.0–0.1) in newborns (8 studies), 0.9% (95% CI 0.8–1.0) in pregnant women/childbearing-age women (47 studies), 1.6% (95% CI 1.2–2.0) in the general population (24 studies), and 2.5% (95% CI 1.0–4.0) in other groups (e.g., sick people) (6 studies). Again, the population-type subgroup analysis demonstrated a high heterogeneity (I2 = 98.8%, p < 0.001; Q = 7577.96 (d.f. = 88), p < 0.001) and degree of publication bias (Egger’s test = 26.02, p < 0.001) among the 88 studies considered.

3.3. Identification of Risk Factors

Thirty studies reported data from 23 countries on risk factors for T. gondii infection (Supplementary Table S2). Among those, one study was multicentric, involving five countries (Belgium, Denmark, Italy, Switzerland, and Norway) from the North, South, and West areas [11], and two studies were undertaken in two East countries (Czech Republic and Slovakia) [168], and in three North countries (Sweden, Estonia, and Iceland) [23]. Among such heterogeneous studies, eight main risk factors were reported in Europe (Figure 3); within those, the most frequently investigated were “contact with cats” (63% [19/30] of studies), “consumption of raw (or undercooked) meat” without specification of the animal species of origin (60% [18/30]), “specific occupation of risk and working with animals” (47% [14/30]), and “contact with soil” (43% [13/30]); nevertheless, within each risk factor category and attending to the frequency/proportion of studies presenting associated statistical significance, “contact with soil” (9/13 [70%] studies), “intake of undercooked beef” (4/6 [66%] studies), and “intake of unwashed vegetables and fruits” (5/8 [63%] studies) stood out as demonstrated main facts associated with seroconversion and infections in European residents.

4. Discussion

The present study aimed at summarizing the anti-Toxoplasma IgG and IgM seroprevalence data of human populations residing in Europe contained in studies published between 2000 and 2020. Previous reviews [169,170,171,172] accomplished this task from a global point of view. In general, remarkable differences in the seroprevalence against T. gondii in different areas and continents were reported, in agreement with the fact that major routes of transmission differ in distinct human contexts involving different cultures, socioeconomic development, and culinary habits.
The present review evidences a pooled overall seroprevalence in European residents (IgG: 32.1%; IgM: 0.6%) that is in the line with other international studies and areas of similar socioeconomic status (and habits). Comparable studies in the general population of the USA between 2011 and 2014 estimated that seroprevalence reached a low level of 11.14% (95% CI: 9.88–12.51) for IgG antibodies [173]. Indeed, an overall IgG seroprevalence of 17.5% in USA/Canada has been reported (reviewed in [171]).
Despite being beyond the scope of the present review, a more specific systematic review [174] focused on the global prevalence of latent toxoplasmosis in pregnant women. The authors reported 31.2% seropositivity in European pregnant women (from 1988 to 2019), which is in agreement with data reported here (e.g., 28.3% in the present review). Nevertheless, current occurrences (e.g., last 5 years) may be lower, since the epidemiological situation has clearly evolved with the evidence provided by several long-term observational studies. Two of these deserve attention: a French survey focused on pregnant women reported a decrease in IgG prevalence from 55.0% in 1995 to 33.7% in 2016 [175], and another comprehensive investigation from Austria reported a yearly decline in IgG seroprevalence of 0.56% in the time period 1995–2006, and a 1.20% annual decline from 2006 to 2012; in sum, IgG seroprevalence decreased from 43.3% in 1995 to 31.5% in 2012 [43]. Both countries have a well-established national surveillance system [176]. As a consequence, national (local/regional) longitudinal studies in different population strata (e.g., health workers, children, etc.) are clearly necessary to assess the true expected decreasing trends in the remaining European countries.
One limitation of the present review is that the mean age of female participants from each study was unknown. This demographic nuance may create the illusion of deflated prevalence rates among pregnant women in specific areas. Therefore, readjustments of the prevalence to standard ages through mathematical procedures would have been desirable to overcome such a bias [177,178].
As usually reported, the presence of IgM is investigated as an indicator of recent Toxoplasma infection, which is the rationale for the majority (66%) of surveys targeting pregnant women or newborn children (Table 3). The seroprevalence values observed in European regions (range: 0.1–1.1%) are in accord with other areas of similar sociodemographic level, such as the USA (1.16% (95% CI: 0.94–1.42) [173]. Despite IgM figures being of epidemiological interest, additional extra effort should be made in many countries to estimate the incidence of clinical toxoplasmosis and its further report (e.g., congenital toxoplasmosis) [8].
Detailed and harmonized data compilation results are of great interest for comparisons among areas, but especially when comprehensive data analyses (e.g., association by logistic regression models) are desired [2,179,180]. In this regard, the lack of harmonization especially among the available serological diagnostic methods [181] can hinder the possibilities of making comparisons between studies; this is a fact that is frequently observed in other meta-analyses, in which the heterogeneity values observed used to be high (>75%) [20,174].
Despite the remarkable degree of heterogeneity observed, the frequency of exposure to T. gondii is also high and widespread; therefore, unraveling the most common route of infection is highly desirable to design appropriate intervention strategies.
Currently, the relative importance of meat-borne vs. oocyst-driven transmission of T. gondii is little known. A review of the literature indicates that 30–60% of infections could be attributed to meat as the infection source, while 6–17% could be attributed to contact with soil or other environmental matrices containing oocysts [11,15,182]. Therefore, studies aiming to unravel what the main sources of infection are for European residents are of major interest [14,16].
Systematically compiling the information is key for the identification of patterns related to toxoplasmosis outbreaks [15,172,183]. Whether the severity of clinical infections in humans is associated with one of such routes is not known; however, in laboratory animals, oocysts, as a source of infection, cause more severe clinical disease [172]. A worldwide systematic review of T. gondii outbreaks [183] selected 38 studies reporting details regarding epidemiological data and dynamic of infections. Some findings deserve attention, notably, a large number of individuals were affected when oocysts were the suspected or confirmed source of infection, and a broader and prolonged appearance of new cases occurred via such a source when compared to tissue cysts. There is limited information regarding Europe, where very few outbreaks have been observed, which were associated with ingestion of unpasteurized milk [184] and undercooked meat [185,186,187].
More recently, additional data on the patterns of transmission and source of infection in global outbreaks of human toxoplasmosis have been reported [15]; authors suggested that transmission routes presented variations by decade. For example, in the 1960s and 1990s, ingestion of cysts in meat and meat products were considered the main sources of infection; in the 1980s, milk contaminated with tachyzoites; in the 2000s, the outbreaks were more related to the presence of oocysts in water, sand, and soil; and after 2010, due to oocysts in raw fruits and vegetables. Therefore, additional studies on the source attribution that aim to identify the true source of infection are warranted [17].
Despite very few toxoplasmosis outbreaks having been reported in Europe [183], exposure to the parasite is frequent, and major risk factors have been identified based on its statistical association with infections. Knowledge of risk factors related to diet, hygiene practices, and lifestyle will help to target prevention efforts. In the present review (Supplementary Table S2), the eight worldwide main risk factors related to the meat-borne and the environmental routes were considered [14]. Among the 30 studies reporting such information in the last 20 years in Europe, three risk factors (“contact with soil”, “consumption of undercooked beef”, and “intake of unwashed vegetables”) stood out as the most frequently associated to seroconversion in people.
Considering those related to the meat-borne route, 66% of studies identified the “intake of undercooked beef” as a risk factor; despite cattle livestock being considered a less susceptible host for T. gondii [1], its meat, unlike others, is frequently (and traditionally) consumed undercooked in Europe. This risk factor had been identified in a worldwide review [12] based on case–control studies aimed at assessing the risk of humans developing acute T. gondii infections; indeed, findings related to the consumption of raw/undercooked beef (OR = 2.22; 95% CI: 1.57–3.12), raw/undercooked sheep meat (OR = 3.85; 95% CI: 1.85–8.00), and unspecified meat (consumption of raw/undercooked meat (OR = 3.44; 95% CI: 1.29–9.16) demonstrated the importance of the meat-borne route. Previous studies carried out prior to the 2000s in Europe identified the “consumption of undercooked beef” (OR = 5.5; 95% CI: 1.1–27) and “consumption of undercooked lamb” (OR = 3.1; 95% CI: 0.85–14) as potential risk factors for primary infections during pregnancy in France [188]; by contrast, for the same segment of the population in Naples (Italy), “consumption of cured pork” (OR = 2.9; 95% CI: 1.6–5.5) and “raw meat” (OR = 2.6; 95% CI: 1.4–4.7) were the most significant elements [189]. In the same target population, “eating raw or undercooked minced meat products” (OR = 4.1; 95% CI: 1.5–11.2), “eating raw or undercooked mutton” (OR = 11.4; 95% CI: 2.1–63.1), and “eating raw or undercooked pork” (OR = 3.4; 95% CI: 1.1–10.4), were recognized in Norway [190]. Finally, in the USA, an area of similar socioeconomic development like Europe, very close factors like “eating raw ground beef” (OR = 6.67; 95% CI: 2.09–21.24), “eating rare lamb” (OR = 8.39; 95% CI: 3.68–19.16), and “eating locally produced cured, dried, or smoked meat” (OR = 1.97; 95% CI: 1.18–3.28) were identified through a case–control study [191].
Nevertheless, in the present review, consumption of other products of animal origin (raw eggs, and unpasteurized milk) was proven to be a non-significant risk factor, unlike in other areas such as the USA where drinking unpasteurized goat’s milk was a risk factor (OR = 5.09; 95% CI: 1.45–17.80) [191] and has been recognized as a cause of outbreaks [183].
Among the risk factors related to the environmental route [192], “contact with soil” and “intake of unwashed vegetables and fruits” were the most frequently identified (70% and 63% of studies, respectively) in the present review; both are related to T. gondii oocysts contamination [16] that is the product of sexual multiplication of the parasite in the gut of felines, which is quite resistant to environmental harmful conditions; a single sporulated oocyst is capable of producing the infection [1]. In European studies prior to 2000, “frequent consumption of raw vegetables outside the home” (OR = 3.1; 95% CI: 1.2–7.7) [188] and “eating unwashed raw vegetables or fruits” (OR = 2.4; 95% CI: 1.1–5.6) [190] had also been identified as risk factors. Also, in the USA [191], “eating raw oysters, clams, or mussels” (OR = 2.22; 95% CI, 1.07–4.61; AR, 16%) was significant in a separate model among persons asked this question, reinforcing the importance of environmental routes for human infections as demonstrated during outbreaks investigations [15]. In this regard, the remarkable frequency of detection of T. gondii oocysts in fresh produce, mollusk bivalves, and water bodies worldwide [16] increases research interest to specifically investigate the relative importance of the environmental route vs. the meat-borne route.
Among other recognized risk factors, “contact with cats” was associated with T. gondii infection in 5 of the 19 studies (Supplementary Table S2), where the variable was considered despite the well-established low frequency of cats shedding oocysts at a given time [22]. Such a risk factor had not been considered in previous studies carried out in Europe [189]; however, in the USA, “having three or more kittens” was significantly associated with infections (OR = 27.89; 95% CI: 5.72–135.86) [191]. Despite the epidemiological importance of cats in T. gondii transmission, contact with cats was also not the predominant risk factor for infection in studies carried out in other parts of the world [12,14]; it was not even identified in the first European multicenter study focused on pregnant women residing in six cities of five countries (Belgium, Denmark, Italy, Norway, and Switzerland) [11]. Other risk factors like “gardening” and “traveling out of Europe or the USA” have been recognized as significant [189,190,191]. Finally, the same authors [173] proposed some sociodemographic risk factors via a full logistic regression model (e.g., ethnic origin, place of birth, crowding, etc.); similar studies have been carried out for European populations (e.g., [154]).
As observed in the present review (Supplementary Table S2) for Europe, and in agreement with studies carried out in other geographical scenarios, most investigations focused on recent/primary infections in pregnant women. In a recent review [14] considering 187 case–control, cohort, and cross-sectional studies conducted worldwide between 1983 and 2016, the authors showed a long list of potential risk factors and highlighted the association of T. gondii sporadic infections with a wide range of environmental factors, along with those related to food habits. The authors declared that the main limitation for making inferences from the data (data interpretation) were the broad definition of exposures and the use of serological methods for the case definition. In this very same context, a major limitation arises; most of the worldwide studies reported risk factors related to T. gondii infections without taking the moment of infection into account (e.g., based upon IgG seropositivity) [13]. Indeed, new studies are necessary to clarify the major sources of infections for the human population in the EU. In this regard, a recent paper in the Netherlands [13] identified the importance of hand hygiene, and the need for detailed enquiries (including risk assessment) with specific meat types.
Despite the present review’s focus on risk factors related to both meat-borne and environmental route-derived infections, further studies also addressing neglected risk factors (e.g., injuries caused by animals, sexual contact, etc.) [168,193,194,195] would be of interest.
The interest of regional-specific analyses to identify specific risk factors (e.g., case–control studies with country-specific products [13]) and the implementation of tools like quantitative microbial risk assessment (QMRA) methods [196] will clarify the current epidemiological scenario. Therefore, an integrative analysis from a One Health point of view will be of major interest to unravel and quantify the sources of T. gondii infections for human populations in Europe, which, by contrast, are subject to rapid change.
In summary, several needs are identified: source attributions and updated risk factors studies are missing in most countries under situations of rapid changes in food preferences and trends. A brief summary of each of the elements is presented below.
(a)
There is a lack of seroprevalence data from several countries (e.g., Baltic states).
(b)
Apparent regional differences may be due to the absence of harmonized data (e.g., type of target population), but also due to differences in a country’s culinary customs and sociodemographic development index.
(c)
The high heterogeneity observed indicates the lack of harmonization of approaches (e.g., diagnostic methods) for T. gondii seroprevalence investigations in Europe. Given the high heterogeneity observed in the present study, it is clear that surveillance systems should first be implemented, and then harmonized in European countries [6,7,176].
(d)
Development of up-to-date risk assessment (local/regional) studies taking into consideration particular trends are needed.
The overall results show that a noticeable segment of the European population (one-third) harbors anti-Toxoplasma IgG antibodies. Therefore, exposure to T. gondii seems to be frequent, and should be considered especially among people at risk. However, under the view of scattered and fragmented available data, a harmonized system for Toxoplasma infection surveillance in European countries is missing. In addition, extra efforts should be made to implement updated risk-factor analyses focusing on detailed source attribution in such a dynamic and evolving society, since culinary customs (and preferences) are rapidly changing.

5. Conclusions

Therefore, exposure to T. gondii seems to be frequent among European residents, and should be considered especially among vulnerable people. However, under the view of the scattered and fragmented data available, a harmonized system for Toxoplasma infection surveillance should be implemented in Europe, in order to better estimate the epidemiological scenario regarding T. gondii infection and its potential clinical toxoplasmosis (e.g., congenital toxoplasmosis). In addition, extra effort should be made to implement updated local risk-factor analyses focusing on detailed source attribution in such a dynamic and evolving society, since culinary customs (and preferences) are rapidly changing.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/pathogens12121430/s1, Table S1: PRISMA_2020 _checklist; Table S2: Main characteristics of the risk factor selected studies (n = 30) for Toxoplasma gondii infection in human residents in Europe. Supplementary Figure S1. Forest plot of the seroprevalence of anti-Toxoplasma gondii IgG antibodies by country. Figure has been constructed with IBM SPSS Statistics (Version 29.0, IBM Corp., Armonk, NY, USA). Supplementary Figure S2. Funnel plots of the seroprevalence of anti-Toxoplasma gondii IgG antibodies by each of the variables considered. Supplementary Figure S3. Forest plot of the seroprevalence of anti-Toxoplasma gondii IgM antibodies by country. References [197,198,199] were cited in the Supplementary Materials.

Author Contributions

Conceptualization, R.C.-B. and L.M.O.-M.; methodology, R.C.-B. and S.C.; software, S.C.; formal analysis, R.C.-B., S.C. and A.R.; investigation, R.C.-B., S.M.G., M.Y.S.-F. and S.C.; resources, G.Á.-G. and L.M.O.-M.; data curation, R.C.-B., S.M.G. and A.R.; writing—original draft preparation, R.C.-B. and S.M.G.; writing—review and editing, R.C.-B., S.M.G., M.Y.S.-F., G.Á.-G. and L.M.O.-M.; visualization, R.C.-B. and S.C.; supervision, R.C.-B. and L.M.O.-M.; funding acquisition, G.Á.-G. and L.M.O.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

R.C.B., G.A.G. and L.M.O.M. are part of the TOXOSOURCES consortium supported by funding from the European Union’s Horizon 2020 Research and Innovation Programme under grant agreement No. 773830: One Health European Joint Programme. M.Y.S.-F. is funded by the pre-doctoral grant PRONABEC (Peruvian Government). The authors are also grateful to Ionela Otea, Walter Basso, Petras Prakas, Pavlo Maksimov, and Gereon Schares for kindly providing original documents and accurate translation of texts.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Pathogens 12 01430 g001
Figure 1. Flowchart describing the study design process. Description of the study search and selection for publications related to (A) seroprevalence of IgG and IgM anti-T. gondii antibodies, and (B) risk factors analyses. (*) A secondary search was carried out based on references included in articles examined for eligibility.
Figure 1. Flowchart describing the study design process. Description of the study search and selection for publications related to (A) seroprevalence of IgG and IgM anti-T. gondii antibodies, and (B) risk factors analyses. (*) A secondary search was carried out based on references included in articles examined for eligibility.
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Pathogens 12 01430 g002
Figure 2. Pooled seroprevalences of T. gondii IgG (A) and IgM (B) antibodies in European residents between 2000 and 2020. AL (Albania), AU (Austria), BH (Bosnia and Herzegovina), CR (Croatia), CY (Cyprus), CZ (Czech Republic), ES (Spain), ET (Estonia), FL (Finland), GE (Germany), GR (Greece), HU (Hungary), IC (Iceland), IR (Ireland), IT (Italy), MA (North Macedonia), NE (Netherlands), NO (Norway), PO (Poland), PT (Portugal), RO (Romania), RS (Russia), SE (Serbia), SK (Slovakia), SL (Slovenia), SW (Sweden), SZ (Switzerland), UK (United Kingdom).
Figure 2. Pooled seroprevalences of T. gondii IgG (A) and IgM (B) antibodies in European residents between 2000 and 2020. AL (Albania), AU (Austria), BH (Bosnia and Herzegovina), CR (Croatia), CY (Cyprus), CZ (Czech Republic), ES (Spain), ET (Estonia), FL (Finland), GE (Germany), GR (Greece), HU (Hungary), IC (Iceland), IR (Ireland), IT (Italy), MA (North Macedonia), NE (Netherlands), NO (Norway), PO (Poland), PT (Portugal), RO (Romania), RS (Russia), SE (Serbia), SK (Slovakia), SL (Slovenia), SW (Sweden), SZ (Switzerland), UK (United Kingdom).
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Figure 3. Summary of the risk factors identified for T. gondii infection in human populations residing in Europe. Each bar indicates the number of studies that considered such potential risk factors and the numbers of them resulting in a statistical association were evaluated with odds ratio or relative risk. Brackets indicate the proportions of studies considering such factors as statistically significant (p < 0.05). Raw data are presented in Supplementary Table S2.
Figure 3. Summary of the risk factors identified for T. gondii infection in human populations residing in Europe. Each bar indicates the number of studies that considered such potential risk factors and the numbers of them resulting in a statistical association were evaluated with odds ratio or relative risk. Brackets indicate the proportions of studies considering such factors as statistically significant (p < 0.05). Raw data are presented in Supplementary Table S2.
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Table 1. Summary of selected studies on seroprevalence of anti-T. gondii antibodies (IgG) in European residents published between 2000 and 2020.
Table 1. Summary of selected studies on seroprevalence of anti-T. gondii antibodies (IgG) in European residents published between 2000 and 2020.
Region/CountryYearPopulationSerological Method *Commercial/In-HouseSamplesReference
Total
(n)		Positive (%)
North
Estonia1999–2001General populationELISACM215118 (54.88)[23]
2004–2011General population ELISACM999557 (55.75)[24]
2004–2011OtherELISACM925539 (58.27)
Finland2000–2001General population MEIA, ELISACM62501231 (19.69)[25,26]
2009OtherELFACM29443 (14.62)[27]
Iceland1999–2001General populationELISACM44043 (9.77)[23,28]
IrelandNRPregnant womenMATIn-house20,2524991 (24.64)[29]
Norway1992–1994Pregnant womenELISACM29,9122937 (9.81)[30]
1994–2005OtherELISACM1073124 (11.55)[31]
2000Pregnant womenNRNR36143 (11.91)[32]
2003Other ELISACM62050 (8.06)[33]
2009Pregnant womenMEIACM20635 (16.99)[34]
2010–2011Pregnant womenELISACM1922179 (9.31)[35]
Sweden1997–1998Pregnant womenMEIACM40,9787390 (18.03)[36,37]
1999–2001General populationELISACM36183 (22.99)[23]
United Kingdom1999OtherDATCM425191 (44.94)[38]
1999–2001Pregnant womenMEIACM1897172 (9.06)[39]
2006–2008Pregnant womenELISACM2610452 (17.31)[40]
2006–2009OtherELISAIn-house1403185 (13.18)[41]
2012–2015General populationELFACM5787930 (16.07)[42]
West
Austria1995–2012Pregnant womenSeveralIn-house, CM10,33163864 (37.39)[43]
2000Other IFATIn-house6032 (53.33)[44]
2000–2007Pregnant womenIFATIn-house, CM63,41620,103 (31.70)[45]
2001–2002Pregnant womenSFIn-house55451830 (33.00) [46]
Belgium1991–2001Pregnant womenNRNR16,5418049 (48.66)[47]
France1995Pregnant women NRNR10,8396806 (62.79)[48]
1995, 2003, 2010OtherNRNR42,88619,015 (44.33)[49]
1997–2013General populationELISACM21,48012,914 (60.12)[50]
2000OtherNRNR26250 (19.08)[51]
2004OtherELISACM273128 (46.88)[52]
2008–2009General populationSeveralCM20601141 (55.38)[53]
Germany2008–2011General populationELFACM65643602 (54.87)[54]
2008–2011Pregnant womenELISACM54021856 (34.35)[55]
Netherlands1995–1996General populationELISAIn-house75213046 (40.49)[56]
2006–2007General populationELISAIn-house55411441 (26.00)[57]
Switzerland1982–1999OtherIFATCM64,6221806 (2.79)[58]
2000–2010OtherELISACM54,216749 (1.38)[59]
East
Czech Republic1988–2006OtherSeveralIn-house, CM626268 (42.81)[60]
1988–2012OtherMEIACM1130474 (41.94)[61]
2000–2004OtherSeveralCM3250757 (23.29)[62]
NRGeneral populationELISACM29093 (32.06)[63]
NRPregnant womenNRNR14423 (15.97)[64]
OtherNRNR14423 (15.97)
Hungary1987–2000Pregnant womenSeveralIn-house, CM31,75918,420 (55.99)[65]
Poland1991–2000General populationSeveralIn-house, CM96615297 (54.82)[66]
1996–1999OtherMEIACM985532 (54.01)[67]
1998Pregnant womenMEIACM1920837 (43.59)[68]
1998–2000OtherDATCM268419 (0.70)[69]
1998–2003Pregnant womenSeveralCM49162030 (41.29)[70]
2000Pregnant womenMEIACM2016722 (35.81)[71]
2000–2003General populationMEIACM46822574 (54.97)[72]
2003–2005OtherELISACM784490 (62.50)[73]
2004–2012Pregnant womenELFACM82813364 (40.62)[74]
2005General populationSeveralIn-house, CM991590 (59.53)[75]
2007–2010Pregnant women MEIACM5528 (50.90)[76]
2008OtherELFACM537292 (54.37)[77]
2010–2012OtherIFATIn-house16993 (55.02)[78]
2013–2014General populationNRNR664445 (67.01)[79]
2013–2014OtherNRNR7437 (50.00)
2014–2015OtherDATCM14857 (38.51)[80]
2015–2016OtherNRNR537103 (19.18)[81]
2016–2017Pregnant womenNRNR628124 (19.74)[82]
2017Other ELFACM373166 (44.50)[83]
NROtherDATIn-house1497864 (57.71)[84]
NRGeneral populationDATIn-house6134 (55.73)[85]
NROtherDATIn-house10770 (65.42)
NRGeneral populationELFACM293186 (63.48)[86]
NROtherIFATIn-house19077 (40.52)[87]
Romania2001–2006Pregnant womenELISACM24892 (37.09)[88]
2005–2007Pregnant womenELISACM510198 (38.82)[89]
2007General populationSeveralCM1155687 (59.48)[90]
2011General populationDATCM304197 (64.8)[91]
2013OtherELISACM5124 (47.05)[92]
2018OtherLATCM44173 (16.55)[93]
NROtherDATCM184106 (57.60)[94]
Russia1996–2002Pregnant womenNRNR87,09945,373 (52.09)[95]
1997–2006General populationSeveralCM23,0246250 (27.14)[96]
2006–2007OtherNRNR4155139 (3.34)[97]
2012OtherCMIACM774 (5.19)[98]
2013General populationELISACM18156 (30.93)[99]
2015General populationELISACM1272323 (25.39)[100]
Slovakia2000–2004Pregnant womenELISACM656145 (22.1)[101]
2003General populationELISACM508123 (24.21)[102]
2006OtherELISACM11840 (33.89)[103]
2007General populationSeveralIn-house, CM1845577 (31.27)[104]
2011General populationMEIACM806282 (34.98)[105]
NRGeneral populationMEIACM1536322 (20.96)[106]
South
Albania2004–2005Pregnant womenELFACM496241 (48.58)[107]
Bosnia and Herzegovina2015General population DATIn-house32098 (30.62)[108]
Croatia1994–1995General population ELISACM1109423 (38.14)[109]
1994–1996General populationELISACM1464533 (36.4)[110]
2000–2001General population MEIACM219115 (52.51)[111]
2000–2001OtherMEIACM16686 (51.80)
2005–2009OtherELFACM502146 (29.08)[112]
Cyprus2009–2011OtherELISACM105669 (6.53)[113]
2009–2014Pregnant womenCMIACM23,0764129 (17.89)
Greece1984, 1994, 2004General populationSeveralIn-house, CM2784851 (30.56)[114]
1985, 1998OtherELISACM469124 (26.43)[115]
1998–2003Pregnant womenELISACM55321628 (29.42)[116]
1998–2005Pregnant womenELISACM12,0003540 (29.50)[117]
Italy1996–2000Pregnant womenELISACM80612773 (34.40)[118]
1996–2000OtherELISACM97305 (0.05)
2001–2012Pregnant womenCMIACM10,2322814 (27.50)[119]
2004–2005Pregnant womenELISACM3426737 (21.51)[120]
2005–2006Pregnant womenELFACM1501281 (18.72)[121]
2005–2006Pregnant womenELFACM892319 (35.76)[122]
2005–2007Pregnant womenELISACM2356564 (23.93)[123]
2007–2009General populationMEIACM10,3522216 (21.40)[124]
2007–2010General populationMEIACM13,1773626 (27.51)[125]
2007–2014Pregnant womenNRNR38,7129368 (24.19)[126]
2009–2018Pregnant womenCMIACM45,4929792 (21.52)[127]
2009–2011Pregnant womenMEIACM10,3472308 (22.30)[128]
2010–2013General populationELFACM12,3063476 (28.24)[129]
2011–2015Other ELFACM33989 (26.25)[130]
2012Pregnant womenNRNR846152 (17.96)[131]
2013–2017OtherELISACM1020169 (16.56)[132]
North Macedonia2004–2005Pregnant womenMEIACM23548 (20.42)[133]
Portugal2000–2015Pregnant womenNRNR40601055 (25.98)[134]
2001–2002, 2013General populationSeveralCM3097913 (29.48)[135]
2004–2009Pregnant womenNRNR3126804 (25.71)[136]
2009–2010OtherCMIACM40198 (24.43)[137]
2010–2011Pregnant womenDATCM15534 (21.93)[138]
Serbia2001–2005OtherDATIn-house765249 (32.54)[139]
2005Pregnant womenMEIACM33497 (29.04)[140]
2011–2012OtherELISACM7919 (24.05)[141]
NRPregnant womenELISACM662180 (27.19)[142]
Slovenia1995–2002OtherIFATIn-house413236 (57.14)[143]
1996–1999Pregnant womenIFATIn-house21,2707151 (33.62)[144]
Spain1987–2001Pregnant womenMEIACM279619 (0.67)[145]
1992–1999Other ELFACM70903009 (42.44)[146]
1992–2008Pregnant womenMEIACM47,63515,196 (31.90)[147]
1999–2000Other SeveralCM15756 (35.66)[148]
1999Pregnant womenNRNR16,3624687 (28.64)[149]
2001Pregnant womenMEIACM2929552 (18.84)[150]
2002–2003General populationMEIACM2660935 (35.15)[151]
2006Pregnant womenELISACM699183 (26.18)[152]
2006Pregnant womenMEIACM2623550 (20.96)[153]
2006–2010Pregnant womenELISACM2933798 (27.20)[154]
2007–2008Pregnant womenELISACM3541602 (17.00)[155]
2007–2008Pregnant womenMEIACM1427433 (30.34)[156]
2007–2010Pregnant womenELISACM80121874 (23.38)[157]
NR: not reported; CM: commercial system/kit; CMIA: chemiluminescent microparticle immunoassay; DAT: direct agglutination test; ELISA: enzyme-linked immunosorbent assay; ELFA: enzyme-linked fluorescence assay; IFAT: immunofluorescent antibody test; MEIA: microparticle enzyme immunoassay; SF: Sabin–Feldman dye test. * Studies included here in which analytical methods were not reported (NR) were selected because of the interest of the whole publication in the specific geographical context (e.g., representativeness).
Table 2. Subgroup analysis for comparison of seroprevalence of anti-T. gondii antibodies (IgG) in European residents published between 2000 and 2020.
Table 2. Subgroup analysis for comparison of seroprevalence of anti-T. gondii antibodies (IgG) in European residents published between 2000 and 2020.
FactorNo. of Studies IncludedPooled Seroprevalence
(95% CI)		Heterogeneity TestEgger’s Test
I2 (%)Q (X2)Q/dfQ-p (p)tp
Area
North1920.1 (16.8–23.5)99.64261.1719<0.0011.140.267
West1738.5 (29.7–47.2)100.01.7 × 10517<0.0014.110.001
East4739.7 (32.1–47.2)99.977,136.8346<0.0011.180.243
South5127.5 (24.4–30.7)99.827,079.8750<0.0012.710.009
Population type
General3838.6 (33.7–43.6)99.817,521.2537<0.0010.790.432
Pregnant women5828.3 (24.2–32.4)99.998,992.7857<0.0010.500.619
Other4731.1 (29.0–33.1)99.953,155.5246<0.0014.70<0.001
Diagnostic method
Commercial10130.2 (28.1–32.3)99.91.8 × 105100<0.0019.66<0.001
In-house1540.1 (35.4–44.8)99.31930.1814<0.0011.490.161
Both843.2 (35.4–51.0)99.97675.927<0.0010.710.507
Overall13432.1 (29.0–35.2)100.03.5 × 105135<0.0016.14<0.001
I2, inverse variance index; Q, Cochran’s X2; Q-p, p-value of Q-tests.
Table 3. Summary of studies reporting anti-T. gondii antibodies (IgM) in European residents published between 2000 and 2020.
Table 3. Summary of studies reporting anti-T. gondii antibodies (IgM) in European residents published between 2000 and 2020.
Region/CountryYearPopulationSerological Method *Commercial/In-HouseSamplesReference
Total (n)Positive (%)
North
Denmark1999–2002NewbornsISAGACM262,91296 (0.04)[158]
1999–2007NewbornsISAGACM547,820100 (0.02)[159]
Norway1992–1994Pregnant womenELISACM35,94047 (0.13)[30]
Sweden1997–1998NewbornsISAGA, ELISACM40,97845 (0.11)[160]
1997–1998NewbornsMEIACM40,9783 (0.01)[37]
United Kingdom1999–2001Pregnant womenMEIACM189712 (0.63)[39]
West
Austria1995–2012Pregnant womenELFA, MEIACM103,316878 (0.85)[43]
2000–2005Pregnant womenELFACM51,75451 (0.10)[161]
2000–2007Pregnant womenELFACM63,41666 (0.10)[45]
2001–2002Parturient womenNR-55457 (0.13)[46]
Belgium1991–2001Pregnant womenNR-16,5418 (0.05)[47]
France2004General populationELISACM2730 (0.00)[52]
Germany2008–2011Pregnant womenELISACM401117 (0.42)[55]
Netherlands2006NewbornsISAGACM10,00818 (0.18)[162]
Switzerland1986–1999Women giving birthELFACM64,622107 (0.16)[58]
2000–2015Women giving birthELISA, MEIACM54,21651 (0.09)[59]
East
Czech Republic1988–2006Other (HIV+ patients)ELISACM6265 (8.06)[60]
2000–2004OtherCFT, ELISACM32501 (0.03)[62]
Hungary1987–2000Pregnant womenELISACM31,75920 (0.06)[65]
Poland1996–1998NewbornsELFA, ELISACM27,51613 (0.05)[163]
1996–1999Women of childbearing ageMEIACM9859 (0.91)[67]
1998–2000NewbornsELISACM268415 (0.56)[69]
1998Pregnant womenMEIACM192027 (1.41)[68]
1998–2003Pregnant womenELISACM4916244 (4.96)[70]
1999–2000-2003General population MEIACM4594196 (4.27)[72]
2000Pregnant womenELFACM20165 (0.25)[71]
2003–2005General population MEIACM78418 (2.29)[73]
2004–2012Pregnant womenELFACM8281803 (9.70)[74]
2007–2010Pregnant womenMEIACM5518 (32.73)[76]
2008General populationELFACM5376 (1.12)[77]
2015–2016Other (Transplant recipients)NR-2923 (1.03)[81]
2016–2017Pregnant womenNR-6282 (0.32)[82]
2017Other (Veterinarians)ELFACM3738 (2.14)[83]
NROtherISAGACM14973 (0.20)[84]
NROtherELFACM1073 (2.80)[85]
NRGeneral populationELFACM610 (0.00)[85]
NRGeneral populationELFACM2935 (1.71)[86]
NRChildren (8–16 yrs)ELISACM1903 (1.57)[87]
Romania2001–2006Pregnant womenELISACM2484 (1.61)[88]
2005–2007Pregnant womenELISACM51046 (9.02)[89]
2007General populationELISA, MEIACM11551 (0.09)[90]
2013Other (Hematological malignancies)ELISACM510 (0.00)[92]
Russia1996–2002Pregnant womenNR-87,0991707 (1.96)[95]
2012General population MEIACM770 (0.00)[98]
Slovakia2000–2004Pregnant womenMEIACM6563 (0.46)[101]
2003General populationMEIACM5080 (0.00)[102]
2007General populationMEIACM18459 (0.49)[104]
South
Albania2004–2005Pregnant womenELFACM4963 (0.60)[107]
Croatia2000–2001General populationMEIACM2192 (0.91)[111]
2000–2001Other (HIV+ patients)MEIACM1662 (1.20)[111]
2005–2009Women of childbearing ageELFACM50212 (2,39)[112]
Cyprus2008–2011High school females (16–18 yrs)ELISACM105610 (0.95)[113]
2009–2011Pregnant womenELISACM17,631107 (0.60)
Greece1984–2004General populationMEIACM278442 (1.51)[114]
1998–2003Pregnant womenELISACM5532185 (3.34)[116]
1998–2005Pregnant womenELISACM12,000396 (3.30)[117]
Italy1996–2000Pregnant womenMEIACM8061188 (2.33)[118]
2001–2012Pregnant womenCMIACM10,0859 (0.09)[119]
2001–2012NewbornsNR-738,5881159 (0.16)[164]
2004–2005Pregnant womenELFA, ELISACM342631 (0.90)[120]
2005–2006Pregnant womenELFACM150123 (1.53)[121]
2005–2007Pregnant womenELISACM2356113 (4.80)[123]
2007–2009General populationELFACM10,352111 (1.07)[124]
2007–2010General populationMEIACM13,177217 (1.65)[125]
2007–2014Women giving birthNR-38,712110 (0.28)[126]
2009–2011Pregnant womenELISACM10,34780 (0.77)[128]
2009–2018Women giving birthCMIACM45,492123 (0.27)[127]
2010–2013General populationELFACM12,306164 (1.33)[129]
2011–2015Pediatric patients ISAGA, MEIACM1874 (2.14)[130]
2012Pregnant womenNR-8463 (0.35)[131]
2012–2014Pregnant womenCMIA, ELFACM36,877156 (0.42)[165]
NRPregnant womenNR-8927 (0.78)[122]
Portugal2000–2015NewbornsNR-39,58522 (0.05)[134]
2004–2009Pregnant womenNR-31265 (0.16)[136]
2009–2010Women of childbearing ageCMIACM4014 (1.00)[137]
2010–2011Pregnant womenDATCM15517 (10.97)[138]
Serbia2001–2005Women of childbearing ageELISA, ISAGACM76553 (6.93)[139]
2004–2008General populationISAGACM110677 (6.96)[166]
2005Pregnant womenMEIACM3344 (1.20)[140]
2011–2012Women of childbearing ageELISACM799 (11.39)[141]
NRPregnant womenELISACM66213 (1.96)[142]
Slovenia1995–2002Other (Ocular disease patients)ELISACM41318 (4.36)[143]
1996–1999Pregnant womenELISACM21,270132 (0.62)[144]
1999–2004Pregnant womenELFACM40,081153 (0.38)[167]
Spain1987–2001Pregnant womenELISA, MEIACM279619 (2.40)[145]
1992–2008Pregnant womenISAGA, MEIACM47,63524 (0.05)[147]
1999Pregnant womenNR-16,362106 (0.65)[149]
1999–2000Other (HIV+ patients)MEIACM1571 (1.75)[148]
2001Pregnant womenMEIACM292924 (0.82)[150]
2006Pregnant womenMEIACM24168 (0.33)[153]
2007–2008Pregnant womenMEIACM142712 (0.84)[156]
NR: not reported; CM: commercial system/kit; CFT: complement fixation test; CMIA: chemiluminescent microparticle immunoassay; ISAGA: immunosorbent agglutination assay; ELFA: enzyme-linked fluorescence assay; ELISA: enzyme-linked immunosorbent assay; MEIA: microparticle enzyme immunoassay. * Studies included here in which analytical methods were not reported (NR) were selected because of the interest of the whole publication in the specific geographical context (e.g., representativeness).
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Calero-Bernal, R.; Gennari, S.M.; Cano, S.; Salas-Fajardo, M.Y.; Ríos, A.; Álvarez-García, G.; Ortega-Mora, L.M. Anti-Toxoplasma gondii Antibodies in European Residents: A Systematic Review and Meta-Analysis of Studies Published between 2000 and 2020. Pathogens 2023, 12, 1430. https://doi.org/10.3390/pathogens12121430

AMA Style

Calero-Bernal R, Gennari SM, Cano S, Salas-Fajardo MY, Ríos A, Álvarez-García G, Ortega-Mora LM. Anti-Toxoplasma gondii Antibodies in European Residents: A Systematic Review and Meta-Analysis of Studies Published between 2000 and 2020. Pathogens. 2023; 12(12):1430. https://doi.org/10.3390/pathogens12121430

Chicago/Turabian Style

Calero-Bernal, Rafael, Solange María Gennari, Santiago Cano, Martha Ynés Salas-Fajardo, Arantxa Ríos, Gema Álvarez-García, and Luis Miguel Ortega-Mora. 2023. "Anti-Toxoplasma gondii Antibodies in European Residents: A Systematic Review and Meta-Analysis of Studies Published between 2000 and 2020" Pathogens 12, no. 12: 1430. https://doi.org/10.3390/pathogens12121430

APA Style

Calero-Bernal, R., Gennari, S. M., Cano, S., Salas-Fajardo, M. Y., Ríos, A., Álvarez-García, G., & Ortega-Mora, L. M. (2023). Anti-Toxoplasma gondii Antibodies in European Residents: A Systematic Review and Meta-Analysis of Studies Published between 2000 and 2020. Pathogens, 12(12), 1430. https://doi.org/10.3390/pathogens12121430

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