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Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Parasitology".

Deadline for manuscript submissions: closed (31 March 2022) | Viewed by 33702

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Dr. Gereon R. M. Schares

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Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Epidemiology, National Reference Centre for Toxoplasmosis, Südufer 10, 17493 Greifswald-Insel Riems, Germany
Interests: epidemiology; biology; transmission; humans; livestock animals; wild animals; coccidia; protozoan parasites; zoonotic parasites; Toxoplasma gondii; Neospora spp.; Besnoitia spp.; Hammondia spp.; Cryptosporidium spp.; Sarcocystis spp.; phylogenetics; genotyping diagnosis and epidemiology of Toxoplasma gondii

Dr. Marco Lalle

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Department of Infectious Diseases, Unit of Foodborne and Neglected Parasitic Diseases, European Union Reference Laboratory for Parasites, Istituto Superiore di Sanità, viale Regina Elena 299, 00161 Roma, Italy
Interests: parasitology; Giardia; protein-protein interaction; cell biology; genotyping; Toxoplasma; Molecular Diagnostic

Prof. Dr. Olgica Durkovic-Dakovic

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Guest Editor

Institute for Medical Research, University of Belgrade, Dr. Subotića 4, 11129 Belgrade, Serbia
Interests: infection; malaria; parasitology; Tropical Diseases; parasitic diseases; zoonoses; epidemiology; microbiology; zoonotic diseases; immunology

Special Issue Information

Dear Colleagues,

Toxoplasma gondii is one of the most important zoonotic parasites in the world. Several routes of infection are possible in animals and humans and three different parasitic stages (oocysts, tissue cysts, and tachyzoites) are involved. In addition, a genetically diverse population, consisting of an increasing number of diverse haplogroups with different virulence characteristics for individual infected host species, further complicates our understanding of this parasite’s epidemiology. Moreover, T. gondii has an extremely broad host spectrum and parasitic stages, such as infectious tissue cysts, contaminate edible tissues of meat-producing animals and represent the most important source of human infection. Other sources of infection include viable oocysts, which may contaminate drinking water, fruits and vegetables, and even seafood. Different hosts, host tissues, and host materials, and the large variety of contaminated matrices, including water and vegetables, often make diagnosis and detection a difficult endeavor. Despite continuing efforts, drug options for toxoplasmosis are scarce, often require combinational therapy, result in poor compliance with a spectrum of adverse events, and are unable to eliminate T. gondii cysts from the infected host. Vaccination approaches would be ideal considering the zoonotic nature of toxoplasmosis.

This Special Issue aims to present a collection of articles on novel diagnostic and detection techniques, their improvement, standardization, and harmonization, and their application in studies to elucidate the epidemiology and transmission of T. gondii as well its genetic composition. Studies exploring new promising drug treatment and vaccination approaches, especially in animals, are also welcome.

Dr. Gereon R. M. Schares
Dr. Marco Lalle
Prof. Dr. Olgica Durkovic-Dakovic
Guest Editors

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Keywords

toxoplasmosis
Toxoplasma gondii
detection
diagnosis
serology
molecular diagnosis
epidemiology
genotyping
treatment
drug
vaccine
livestock
wild animals
vegetables
fresh produce
drinking water
seafood

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Published Papers (9 papers)

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12 pages, 1327 KiB

Open AccessArticle

Toxoplasma gondii Serotypes in Italian and Foreign Populations: A Cross-Sectional Study Using a Homemade ELISA Test

by Sara Caldrer, Ambra Vola, Guglielmo Ferrari, Tamara Ursini, Cristina Mazzi, Valeria Meroni and Anna Beltrame

Microorganisms 2022, 10(8), 1577; https://doi.org/10.3390/microorganisms10081577 - 5 Aug 2022

Cited by 1 | Viewed by 3190

Abstract

Toxoplasma gondii is a protozoan parasite responsible for human toxoplasmosis. The three major clonal lineages and different recombinant strains of T. gondii have a varied global distribution. This study aimed at evaluating the epidemiological distribution of types II and I–III and recombinant or mixed T. gondii in Italians and foreigners residing in Italy, establishing an association between serotypes and demographic characteristics. We collected the sera of 188 subjects who had tested positive for specific T. gondii antibodies. The population was differentiated into groups based on sex, nationality, and place of birth (Italy, Africa, South America, Asia, or Europe (except Italy)). We then performed a homemade ELISA test that detected both the antibodies against the amino acid sequences of the three main genotype antigens (I–III) in human sera and discerned the T. gondii strains. Serotype II of T. gondii was the most prevalent in the Italian population, whereas type I–III was the most prevalent in the foreign group. Surprisingly, we observed a notable amount of recombinant or mixed serotypes in European and Italian subjects. Moreover, we showed a significant difference in the prevalence of T. gondii serotypes between men and women, Italians, and foreigners. This descriptive study is the first to investigate the epidemiological distribution of T. gondii serotypes in humans in Italy using a homemade ELISA. We considered this technique suitable for discriminating between serotypes II and I–III and, consequently, for an epidemiological study focusing on the observation of circulating T. gondii strains and clinical correlations. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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14 pages, 1001 KiB

Open AccessArticle

Seroprevalence, Direct Detection and Risk Factors for Toxoplasma gondii Infection in Pigs in Serbia, and Influence of Biosecurity Measures

by Nikola Betić, Nedjeljko Karabasil, Olgica Djurković-Djaković, Vladimir Ćirković, Branko Bobić, Ivana Branković Lazić, Vesna Djordjević and Ivana Klun

Microorganisms 2022, 10(5), 1069; https://doi.org/10.3390/microorganisms10051069 - 23 May 2022

Cited by 4 | Viewed by 2308

Abstract

Consumption of Toxoplasma gondii contaminated pork is a major risk factor for human infection. We thus conducted a cross-sectional survey on the seroprevalence of T. gondii infection in a representative sample of slaughter pigs from throughout Serbia and examined the influence of farm biosecurity-related risk factors on infection. In addition, direct detection of the parasite (by mouse bioassay) or its DNA was performed in the hearts of a subset of seropositive sows. The overall seroprevalence in the sample of 825 pigs as determined by the modified agglutination test (MAT) was 16.5%. Older age and inadequate rodent control were independent infection risk factors for pigs. In a subset of 581 pigs with complete biosecurity-related data, in addition to older age, smallholders’ finishing type farms (as opposed to farrow-to-finish), multispecies farming, and origin from Western and Central and South-Eastern Serbia (vs. the Northern region), all increased the risk of infection, while the absence of disinfection boot-dips in front of each barn and Belgrade district origin (vs. the Northern region) were associated with a 62% and 75% lower risk of infection, respectively. Evidence of viable parasites was obtained in 13 (41.9%) of the 31 bioassayed sow hearts, of which by isolation of brain cysts in seven, by detection of T. gondii DNA in an additional four, and by serology in another two. Recovery of brain cysts mostly (5/7) from sows with a MAT titre of ≥1:100 indicates the risk for consumers. These results highlight the public health risk from pork consumption and point to mandatory use of professional rodent control services, abstaining from multispecies farming, keeping disinfection boot-dips clean and freshly refilled, as well as strict implementation of zoo-hygienic measures on smallholders’ farms as specific farm biosecurity measures needed for its reduction. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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8 pages, 269 KiB

Open AccessArticle

Seroepidemiology of Toxoplasma gondii Infection in Blood Donors from Western Romania

by Maria Alina Lupu, Rodica Lighezan, Ana Alexandra Paduraru, Angela Dragomir, Radu Pavel, Sebastian Grada, Alin Gabriel Mihu, Sorin Ursoniu and Tudor Rares Olariu

Microorganisms 2022, 10(5), 973; https://doi.org/10.3390/microorganisms10050973 - 5 May 2022

Cited by 17 | Viewed by 2529

Abstract

Background: Toxoplasma gondii is estimated to infect 33% of blood donors worldwide, and seroprevalence varies widely between countries. We aimed to evaluate, for the first time, the seroprevalence and risk factors associated with T. gondii in blood donors from Western Romania. Methods: Serologic testing to demonstrate the presence of T. gondii antibodies was conducted in 1347 healthy blood donors. Risk factors for T. gondii infection were assessed through an epidemiological questionnaire. Results: The overall prevalence of T. gondii antibodies was 45.9%, with a significant age-associated increase (p < 0.001) from 32.6% in age group 18–25 years to 67.6% in age group 56–63 years. T. gondii seroprevalence decreased with increasing level of education, from 64.3% in individuals who graduated from elementary/middle school to 40.4% in those who graduated from University (p < 0.001). The multiple logistic regression analysis revealed that age, level of education and having pets (cats and/or dogs) were significantly associated with T. gondii infection. Conclusions: This study brings new and valuable data regarding the seroepidemiology of T. gondii infection in Romania. Our findings indicate a high prevalence of T. gondii antibodies in blood donors and may serve as a starting point for further epidemiological studies that should lead to implementation of prevention programs for toxoplasmosis. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

10 pages, 434 KiB

Open AccessArticle

Epidemiology of Toxoplasmosis in SERBIA: A Cross-Sectional Study on Blood Donors

by Milena Stopić, Tijana Štajner, Ljiljana Marković-Denić, Vladimir Nikolić, Iva Djilas, Snežana Jovanović Srzentić, Olgica Djurković-Djaković and Branko Bobić

Microorganisms 2022, 10(3), 492; https://doi.org/10.3390/microorganisms10030492 - 23 Feb 2022

Cited by 16 | Viewed by 4065

Abstract

Toxoplasmosis is a globally distributed parasitic zoonosis, affecting approximately one third of the human population. Epidemiological studies on toxoplasmosis conducted in Serbia so far have been focused on women of childbearing age, without a clear insight into the prevalence in the general population. We conducted a cross-sectional study in a representative sample of the healthy adult population consisting of 1095 blood donors of both genders to establish the prevalence and risk factors for Toxoplasma gondii infection. Data on the demographic and clinical characteristics of all study participants, as well as on their lifestyle habits, were collected by means of a questionnaire. The overall prevalence of infection was 20.5% (224/1095) and the avidity of the specific IgG antibodies detected was high in a vast majority of the seropositive donors (98.2%). Interestingly, the remaining 1.8% of the specific IgG positive samples were of borderline avidity (4/224), in complete absence of specific IgM. The multivariate logistic regression analysis showed that independent risk factors included age (from OR (95% CI) 1.9 (1.13–3.28) in the 30–39 age group, to 6.8 (3.27–14.24) in the age group of >60 years), suburban living (OR (95% CI) 2.2 (1.43–3.34)) and contact with soil (OR (95% CI) 1.4 (1.01–1.94)). This first large-scale study on toxoplasmosis in the general population in Serbia shows the lowest prevalence ever reported in this country. Moreover, the novel perspective on risk factors provides an updated basis for future prevention programs. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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14 pages, 7829 KiB

Open AccessArticle

Toxoplasma gondii Genotypes Circulating in Serbia—Insight into the Population Structure and Diversity of the Species in Southeastern Europe, a Region of Intercontinental Strain Exchange

by Aleksandra Uzelac, Ivana Klun, Vladimir Ćirković, Neda Bauman, Branko Bobić, Tijana Štajner, Jelena Srbljanović, Olivera Lijeskić and Olgica Djurković-Djaković

Microorganisms 2021, 9(12), 2526; https://doi.org/10.3390/microorganisms9122526 - 7 Dec 2021

Cited by 6 | Viewed by 3160

Abstract

In Europe, Toxoplasma gondii lineage II is dominant, and ToxoDB#1 the most frequently occurring genotype. The abundance of lineage III genotypes varies geographically and lineage I are rare, yet present in several regions of the continent. Data on the T. gondii population structure in southeastern Europe (SEE) are scarce, yet necessary to appreciate the diversity of the species in Europe. To help fill this gap, we genotyped 67 strains from nine species of intermediate hosts in Serbia by MnPCR-RFLP, determined the population structure, and identified the genotypes using ToxoDB. A neighbor-joining tree was also constructed from the isolates genotyped on nine loci. While 42% of the total genotype population consisted of ToxoDB#1 and ToxoDB#2, variant genotypes of both lineages comprised 46% of the population in wildlife and 28% in domestic animals and humans. One genotype of Africa 4 lineage was detected in a human sample. Interestingly, the findings include one lineage III variant and one II/III recombinant isolate with intercontinental distribution, which appear to be moderately related to South American genotypes. Based on these findings, SEE is a region of underappreciated T. gondii genetic diversity and possible strain exchange between Europe and Africa. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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14 pages, 4305 KiB

Open AccessArticle

Effect of 17β-Estradiol, Progesterone, and Tamoxifen on Neurons Infected with Toxoplasma gondii In Vitro

by María de la Luz Galván Ramírez, Judith Marcela Dueñas-Jiménez, Adrián Fernando Gutiérrez-Maldonado and Laura Rocío Rodríguez Pérez

Microorganisms 2021, 9(10), 2174; https://doi.org/10.3390/microorganisms9102174 - 19 Oct 2021

Cited by 1 | Viewed by 2188

Abstract

Toxoplasma gondii (T. gondii) is the causal agent of toxoplasmosis, which produces damage in the central nervous system (CNS). Toxoplasma–CNS interaction is critical for the development of disease symptoms. T. gondii can form cysts in the CNS; however, neurons are more resistant to this infection than astrocytes. The probable mechanism for neuron resistance is a permanent state of neurons in the interface, avoiding the replication of intracellular parasites. Steroids regulate the formation of Toxoplasma cysts in mice brains. 17β-estradiol and progesterone also participate in the control of Toxoplasma infection in glial cells in vitro. The aim of this study was to evaluate the effects of 17β-estradiol, progesterone, and their specific agonists–antagonists on Toxoplasma infection in neurons in vitro. Neurons cultured were pretreated for 48 h with 17β-estradiol or progesterone at 10, 20, 40, 80, or 160 nM/mL or tamoxifen 1 μM/mL plus 17β-estradiol at 10, 20, 40, 80, and 160 nM/mL. In other conditions, the neurons were pretreated during 48 h with 4,4′,4″-(4-propyl-[1H] pyrozole-1,3,5-triyl) trisphenol or 23-bis(4-hydroxyphenyl) propionitrile at 1 nM/mL, and mifepristone 1 µM/mL plus progesterone at 10, 20, 40, 80, and 160 nM/mL. Neurons were infected with 5000 tachyzoites of the T. gondii strain RH. The effect of 17β estradiol, progesterone, their agonists, or antagonists on Toxoplasma infection in neurons was evaluated at 24 and 48 h by immunocytochemistry. T. gondii replication was measured with the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide reduction assay. 17β-Estradiol alone or plus tamoxifen reduced infected neurons (50%) compared to the control at 48 h. Progesterone plus estradiol decreased the number of intracellular parasites at 48 h of treatment compared to the control (p < 0.001). 4,4′,4″-(4-propyl-[1H] pyrozole-1,3,5-triyl) trisphenol and 23-bis(4-hydroxyphenyl) propionitrile reduced infected neurons at 48 h of treatment significantly compared to the control (p < 0.05 and p < 0.001, respectively). The Toxoplasma infection process was decreased by the effect of 17β-estradiol alone or combined with tamoxifen or progesterone in neurons in vitro. These results suggest the essential participation of progesterone and estradiol and their classical receptors in the regulation of T. gondii neuron infection. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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Review

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38 pages, 1898 KiB

Open AccessReview

Contamination of Soil, Water, Fresh Produce, and Bivalve Mollusks with Toxoplasma gondii Oocysts: A Systematic Review

by Nadia María López Ureña, Umer Chaudhry, Rafael Calero Bernal, Santiago Cano Alsua, Davide Messina, Francisco Evangelista, Martha Betson, Marco Lalle, Pikka Jokelainen, Luis Miguel Ortega Mora and Gema Álvarez García

Microorganisms 2022, 10(3), 517; https://doi.org/10.3390/microorganisms10030517 - 27 Feb 2022

Cited by 17 | Viewed by 6139

Abstract

Toxoplasma gondii is a major foodborne pathogen capable of infecting all warm-blooded animals, including humans. Although oocyst-associated toxoplasmosis outbreaks have been documented, the relevance of the environmental transmission route remains poorly investigated. Thus, we carried out an extensive systematic review on T. gondii oocyst contamination of soil, water, fresh produce, and mollusk bivalves, following the PRISMA guidelines. Studies published up to the end of 2020 were searched for in public databases and screened. The reference sections of the selected articles were examined to identify additional studies. A total of 102 out of 3201 articles were selected: 34 articles focused on soil, 40 focused on water, 23 focused on fresh produce (vegetables/fruits), and 21 focused on bivalve mollusks. Toxoplasma gondii oocysts were found in all matrices worldwide, with detection rates ranging from 0.09% (1/1109) to 100% (8/8) using bioassay or PCR-based detection methods. There was a high heterogeneity (I² = 98.9%), which was influenced by both the sampling strategy (e.g., sampling site and sample type, sample composition, sample origin, season, number of samples, cat presence) and methodology (recovery and detection methods). Harmonized approaches are needed for the detection of T. gondii in different environmental matrices in order to obtain robust and comparable results. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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25 pages, 1291 KiB

Open AccessReview

Identification of Oocyst-Driven Toxoplasma gondii Infections in Humans and Animals through Stage-Specific Serology—Current Status and Future Perspectives

by Gema Álvarez García, Rebecca Davidson, Pikka Jokelainen, Siv Klevar, Furio Spano and Frank Seeber

Microorganisms 2021, 9(11), 2346; https://doi.org/10.3390/microorganisms9112346 - 13 Nov 2021

Cited by 14 | Viewed by 4531

Abstract

The apicomplexan zoonotic parasite Toxoplasma gondii has three infective stages: sporozoites in sporulated oocysts, which are shed in unsporulated form into the environment by infected felids; tissue cysts containing bradyzoites, and fast replicating tachyzoites that are responsible for acute toxoplasmosis. The contribution of oocysts to infections in both humans and animals is understudied despite being highly relevant. Only a few diagnostic antigens have been described to be capable of discriminating which parasite stage has caused an infection. Here we provide an extensive overview of the antigens and serological assays used to detect oocyst-driven infections in humans and animals according to the literature. In addition, we critically discuss the possibility to exploit the increasing knowledge of the T. gondii genome and the various ‘omics datasets available, by applying predictive algorithms, for the identification of new oocyst-specific proteins for diagnostic purposes. Finally, we propose a workflow for how such antigens and assays based on them should be evaluated to ensure reproducible and robust results. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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19 pages, 1104 KiB

Open AccessReview

Molecular Methods for the Detection of Toxoplasma gondii Oocysts in Fresh Produce: An Extensive Review

by Iva Slana, Nadja Bier, Barbora Bartosova, Gianluca Marucci, Alessia Possenti, Anne Mayer-Scholl, Pikka Jokelainen and Marco Lalle

Microorganisms 2021, 9(1), 167; https://doi.org/10.3390/microorganisms9010167 - 13 Jan 2021

Cited by 7 | Viewed by 3991

Abstract

Human infection with the important zoonotic foodborne pathogen Toxoplasma gondii has been associated with unwashed raw fresh produce consumption. The lack of a standardised detection method limits the estimation of fresh produce as an infection source. To support method development and standardisation, an extensive literature review and a multi-attribute assessment were performed to analyse the key aspects of published methods for the detection of T. gondii oocyst contamination in fresh produce. Seventy-seven published studies were included, with 14 focusing on fresh produce. Information gathered from expert laboratories via an online questionnaire were also included. Our findings show that procedures for oocyst recovery from fresh produce mostly involved sample washing and pelleting of the washing eluate by centrifugation, although washing procedures and buffers varied. DNA extraction procedures including mechanical or thermal shocks were identified as necessary steps to break the robust oocyst wall. The most suitable DNA detection protocols rely on qPCR, mostly targeting the B1 gene or the 529 bp repetitive element. When reported, validation data for the different detection methods were not comparable and none of the methods were supported by an interlaboratory comparative study. The results of this review will pave the way for an ongoing development of a widely applicable standard operating procedure. Full article

(This article belongs to the Special Issue Advances in the Diagnosis, Detection, Epidemiology, and Control of Toxoplasma gondii)

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