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It is not only the cat that did it: How to prevent and treat congenital toxoplasmosis

  • Florence Robert-Gangneux
    Correspondence
    Corresponding author. Laboratory of Parasitology, Centre Hospitalier Universitaire de Rennes, France.
    Affiliations
    Laboratory of Parasitology, Centre Hospitalier Universitaire de Rennes, France

    INSERM U1085/IRSET (Institut de Recherche en Santé Environnement Travail), Université Rennes 1, France
    Search for articles by this author
Published:October 11, 2013DOI:https://doi.org/10.1016/j.jinf.2013.09.023

      Summary

      The apicomplexan parasite Toxoplasma gondii was discovered a little over one hundred years ago and was soon recognized as a pathogen responsible for congenital infection. But detailed understanding of its epidemiology emerged only after 1970 with the discovery of its life cycle. In the last ten years, high resolution molecular tools have allowed the characterization of various strain types with different virulence patterns, and current studies are exploring the distribution of these different genotypes. In parallel, sophisticated diagnostic tools have been developed and awareness of disease burden has led some European countries with high prevalence rates to implement screening of pregnant women. In this article, the screening options and therapies used to prevent congenital toxoplasmosis are dissected in the light of recent data from cohort studies and other epidemiological data.

      Keywords

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      References

        • Nicolle C.
        • Manceaux L.
        Sur une infection à corps de Leishman (ou organismes voisins) du gondi.
        CR Hebd Séances Acad Sci. 1908; 147: 763-766
        • Dubey J.P.
        • Frenkel J.K.
        Cyst-induced toxoplasmosis in cats.
        J Protozool. 1972; 19: 155-177
        • Hutchison W.M.
        • Dunachie J.F.
        • Siim J.C.
        • Work K.
        Life cycle of Toxoplasma gondii.
        Br Med J. 1969; 4: 806
        • Frenkel J.K.
        • Dubey J.P.
        • Miller N.L.
        Toxoplasma gondii in cats: fecal stages identified as coccidian oocysts.
        Science. 1970; 167: 893-896
        • Dubey J.P.
        The history of Toxoplasma gondii–the first 100 years.
        J Eukaryot Microbiol. 2008 Nov-Dec; 55: 467-475
        • Weiss L.M.
        • Dubey J.P.
        Toxoplasmosis: a history of clinical observations.
        Int J Parasitol. 2009; 39: 895-901
        • Mercier A.
        • Ajzenberg D.
        • Devillard S.
        • Demar M.P.
        • de Thoisy B.
        • Bonnabau H.
        • et al.
        Human impact on genetic diversity of Toxoplasma gondii: example of the anthropized environment from French Guiana.
        Infect Genet Evol. 2011; 6: 1378-1387
        • ElHajj H.
        • Lebrun M.
        • Arold S.T.
        • Vial H.
        • Labesse G.
        • Dubremetz J.F.
        ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii.
        PLoS Pathog. 2007; 3: e14
        • Robert-Gangneux F.
        • Darde M.L.
        Epidemiology of and diagnostic strategies for toxoplasmosis.
        Clin Microbiol Rev. 2012; 25: 264-296
        • Dubey J.P.
        Advances in the life cycle of Toxoplasma gondii.
        Int J Parasitol. 1998; 28: 1019-1024
        • Lunden A.
        • Uggla A.
        Infectivity of Toxoplasma gondii in mutton following curing, smoking, freezing or microwave cooking.
        Int J Food Microbiol. 1992; 15: 357-363
        • Dubey J.P.
        Long-term persistence of Toxoplasma gondii in tissues of pigs inoculated with T. gondii oocysts and effect of freezing on viability of tissue cysts in pork.
        Am J Vet Res. 1988; 49: 910-913
        • Dubey J.P.
        Toxoplasma gondii oocyst survival under defined temperatures.
        J Parasitol. 1998; 84: 862-865
        • Frenkel J.K.
        • Dubey J.P.
        Effects of freezing on the viability of toxoplasma oocysts.
        J Parasitol. 1973; 59: 587-588
        • Tenter A.M.
        • Heckeroth A.R.
        • Weiss L.M.
        Toxoplasma gondii: from animals to humans.
        Int J Parasitol. 2000; 30: 1217-1258
        • Kijlstra A.
        • Jongert E.
        Toxoplasma-safe meat: close to reality?.
        Trends Parasitol. 2009; 25: 18-22
        • Dubey J.P.
        • Jones J.L.
        Toxoplasma gondii infection in humans and animals in the United States.
        Int J Parasitol. 2008; 38: 1257-1278
        • Halos L.
        • Thebault A.
        • Aubert D.
        • Thomas M.
        • Perret C.
        • Geers R.
        • et al.
        An innovative survey underlining the significant level of contamination by Toxoplasma gondii of ovine meat consumed in France.
        Int J Parasitol. 2010; 40: 193-200
        • Dubey J.P.
        Toxoplasmosis of animals and humans.
        2nd ed. 2010 (Boca Raton, F.L.)
        • Montoya J.G.
        • Liesenfeld O.
        Toxoplasmosis.
        Lancet. 2004; 363: 1965-1976
        • Pappas G.
        • Roussos N.
        • Falagas M.E.
        Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis.
        Int J Parasitol. 2009; 39: 1385-1394
        • Villena I.
        • Ancelle T.
        • Delmas C.
        • Garcia P.
        • Brezin A.P.
        • Thulliez P.
        • et al.
        Congenital toxoplasmosis in France in 2007: first results from a national surveillance system.
        Euro Surveill. 2010; 15
        • Berger F.G.V.
        • Le Strat Y.
        • Desenclos J.C.
        Toxoplasmosis in pregnant women in France: trends in seroprevalence and incidence, and associated factors, 1995–2003.
        Bull Epidemiol Hebd. 2008; 14-15: 117-121
        • Guerina N.G.
        • Hsu H.W.
        • Meissner H.C.
        • Maguire J.H.
        • Lynfield R.
        • Stechenberg B.
        • et al.
        Neonatal serologic screening and early treatment for congenital Toxoplasma gondii infection. The New England Regional Toxoplasma Working Group.
        N Engl J Med. 1994; 330: 1858-1863
        • Lago E.G.
        • Neto E.C.
        • Melamed J.
        • Rucks A.P.
        • Presotto C.
        • Coelho J.C.
        • et al.
        Congenital toxoplasmosis: late pregnancy infections detected by neonatal screening and maternal serological testing at delivery.
        Paediatr Perinat Epidemiol. 2007; 21: 525-531
        • Darde M.L.
        • Bouteille B.
        • Pestre-Alexandre M.
        Isoenzyme analysis of 35 Toxoplasma gondii isolates and the biological and epidemiological implications.
        J Parasitol. 1992; 78: 786-794
        • Howe D.K.
        • Sibley L.D.
        Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease.
        J Infect Dis. 1995; 172: 1561-1566
        • Ajzenberg D.
        • Banuls A.L.
        • Tibayrenc M.
        • Dardé M.L.
        Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups.
        Int J Parasitol. 2002; 32: 27-38
        • Ajzenberg D.
        • Banuls A.L.
        • Su C.
        • Dumetre A.
        • Demar M.
        • Carme B.
        • et al.
        Genetic diversity, clonality and sexuality in Toxoplasma gondii.
        Int J Parasitol. 2004; 34: 1185-1196
        • Ajzenberg D.
        • Cogne N.
        • Paris L.
        • Bessieres M.H.
        • Thulliez P.
        • Filisetti D.
        • et al.
        Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings.
        J Infect Dis. 2002; 186: 684-689
        • Aubert D.
        • Ajzenberg D.
        • Richomme C.
        • Gilot-Fromont E.
        • Terrier M.E.
        • de Gevigney C.
        • et al.
        Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France.
        Vet Parasitol. 2010; 171: 346-349
        • Pomares C.
        • Ajzenberg D.
        • Bornard L.
        • Bernardin G.
        • Hasseine L.
        • Darde M.L.
        • et al.
        Toxoplasmosis and horse meat, France.
        Emerg Infect Dis. 2011; 17: 1327-1328
        • Khan A.
        • Dubey J.P.
        • Su C.
        • Ajioka J.W.
        • Rosenthal B.M.
        • Sibley L.D.
        Genetic analyses of atypical Toxoplasma gondii strains reveal a fourth clonal lineage in North America.
        Int J Parasitol. 2011; 41: 645-655
        • Pena H.F.
        • Gennari S.M.
        • Dubey J.P.
        • Su C.
        Population structure and mouse-virulence of Toxoplasma gondii in Brazil.
        Int J Parasitol. 2008; 38: 561-569
        • Mercier A.
        • Devillard S.
        • Ngoubangoye B.
        • Bonnabau H.
        • Banuls A.L.
        • Durand P.
        • et al.
        Additional haplogroups of Toxoplasma gondii out of Africa: population structure and mouse-virulence of strains from Gabon.
        PLoS Negl Trop Dis. 2010; 4: e876
        • Zhou P.
        • Nie H.
        • Zhang L.X.
        • Wang H.Y.
        • Yin C.C.
        • Su C.
        • et al.
        Genetic characterization of Toxoplasma gondii isolates from pigs in China.
        J Parasitol. 2010; 96: 1027-1029
        • Carme B.
        • Bissuel F.
        • Ajzenberg D.
        • Bouyne R.
        • Aznar C.
        • Demar M.
        • et al.
        Severe acquired toxoplasmosis in immunocompetent adult patients in French Guiana.
        J Clin Microbiol. 2002; 40: 4037-4044
        • Silveira C.
        • Belfort Jr., R.
        • Burnier Jr., M.
        • Nussenblatt R.
        Acquired toxoplasmic infection as the cause of toxoplasmic retinochoroiditis in families.
        Am J Ophthalmol. 1988; 106: 362-364
        • Silva C.S.
        • Neves Ede S.
        • Benchimol E.I.
        • Moraes D.R.
        Postnatal acquired toxoplasmosis patients in an infectious diseases reference center.
        Braz J Infect Dis. 2008; 12: 438-441
        • Delair E.
        • Monnet D.
        • Grabar S.
        • Dupouy-Camet J.
        • Yera H.
        • Brezin A.P.
        Respective roles of acquired and congenital infections in presumed ocular toxoplasmosis.
        Am J Ophthalmol. 2008; 146: 851-855
        • Elbez-Rubinstein A.
        • Ajzenberg D.
        • Darde M.L.
        • Cohen R.
        • Dumetre A.
        • Yera H.
        • et al.
        Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review.
        J Infect Dis. 2009; 199: 280-285
        • Bahia-Oliveira L.M.
        • Jones J.L.
        • Azevedo-Silva J.
        • Alves C.C.
        • Orefice F.
        • Addiss D.G.
        Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state.
        Brazil Emerg Infect Dis. 2003; 9: 55-62
        • Balasundaram M.B.
        • Andavar R.
        • Palaniswamy M.
        • Venkatapathy N.
        Outbreak of acquired ocular toxoplasmosis involving 248 patients.
        Arch Ophthalmol. 2010; 128: 28-32
        • Bowie W.R.
        • King A.S.
        • Werker D.H.
        • Isaac-Renton J.L.
        • Bell A.
        • Eng S.B.
        • et al.
        Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma Investigation Team.
        Lancet. 1997; 350: 173-177
        • Jones J.L.
        • Dubey J.P.
        Waterborne toxoplasmosis – recent developments.
        Exp Parasitol. 2010; 124: 10-25
        • Jones J.L.
        • Dargelas V.
        • Roberts J.
        • Press C.
        • Remington J.S.
        • Montoya J.G.
        Risk factors for Toxoplasma gondii infection in the United States.
        Clin Infect Dis. 2009; 49: 878-884
        • Benard A.
        • Petersen E.
        • Salamon R.
        • Chene G.
        • Gilbert R.
        • Salmi L.R.
        Survey of European programmes for the epidemiological surveillance of congenital toxoplasmosis.
        Euro Surveill. 2008; 13
        • Leroy V.
        • Pierre-Alain Raeber P.A.
        • Petersen
        • Salmi L.R.
        • Kaminski M.
        • Villena I.
        • et al.
        • for the Eurotoxo Group (Panel 3)
        National public health policies and routines programs to prevent congenital toxoplasmosis, Europe, 2005.
        ([Unpublished report]) The Eurotoxo Group, Bordeaux (France)2005
        • Wallon M.
        • Franck J.
        • Thulliez P.
        • Huissoud C.
        • Peyron F.
        • Garcia-Meric P.
        • et al.
        Accuracy of real-time polymerase chain reaction for Toxoplasma gondii in amniotic fluid.
        Obstet Gynecol. 2010; 115: 727-733
      1. Centre National de Référence de la Toxoplasmose. http://cnrtoxoplasmose.chu-reims.fr/?page_id=224.

        • Wallon M.
        • Liou C.
        • Garner P.
        • Peyron F.
        Congenital toxoplasmosis: systematic review of evidence of efficacy of treatment in pregnancy.
        BMJ. 1999; 318: 1511-1514
        • Gilbert R.
        • Gras L.
        Effect of timing and type of treatment on the risk of mother to child transmission of Toxoplasma gondii.
        BJOG. 2003; 110: 112-120
        • Thiebaut R.
        • Leproust S.
        • Chene G.
        • Gilbert R.
        Effectiveness of prenatal treatment for congenital toxoplasmosis: a meta-analysis of individual patients' data.
        Lancet. 2007; 369: 115-122
        • Wallon M.
        • Peyron F.
        • Cornu C.
        • Vinault S.
        • Abrahamowicz M.
        • Kopp C.B.
        • et al.
        Congenital toxoplasma infection: monthly prenatal screening decreases transmission rate and improves clinical outcome at age 3 years.
        Clin Infect Dis. 2013; 56: 1223-1231
        • Gras L.
        • Wallon M.
        • Pollak A.
        • Cortina-Borja M.
        • Evengard B.
        • Hayde M.
        • et al.
        Association between prenatal treatment and clinical manifestations of congenital toxoplasmosis in infancy: a cohort study in 13 European centres.
        Acta Paediatr. 2005; 94: 1721-1731
        • Cortina-Borja M.
        • Tan H.K.
        • Wallon M.
        • Paul M.
        • Prusa A.
        • Buffolano W.
        • et al.
        Prenatal treatment for serious neurological sequelae of congenital toxoplasmosis: an observational prospective cohort study.
        PLoS Med. 2010; 7
        • Hotop A.
        • Hlobil H.
        • Gross U.
        Efficacy of rapid treatment initiation following primary Toxoplasma gondii infection during pregnancy.
        Clin Infect Dis. 2012; 54: 1545-1552
        • Foulon W.
        • Villena I.
        • Stray-Pedersen B.
        • Decoster A.
        • Lappalainen M.
        • Pinon J.M.
        • et al.
        Treatment of toxoplasmosis during pregnancy: a multicenter study of impact on fetal transmission and children's sequelae at age 1 year.
        Am J Obstet Gynecol. 1999; 180: 410-415
        • Kieffer F.
        • Wallon M.
        • Garcia P.
        • Thulliez P.
        • Peyron F.
        • Franck J.
        Risk factors for retinochoroiditis during the first 2 years of life in infants with treated congenital toxoplasmosis.
        Pediatr Infect Dis J. 2008; 27: 27-32
        • Gilbert R.
        • Tan H.K.
        • Cliffe S.
        • Guy E.
        • Stanford M.
        Symptomatic toxoplasma infection due to congenital and postnatally acquired infection.
        Arch Dis Child. 2006; 91: 495-498
        • Stillwaggon E.
        • Carrier C.S.
        • Sautter M.
        • McLeod R.
        Maternal serologic screening to prevent congenital toxoplasmosis: a decision-analytic economic model.
        PLoS Negl Trop Dis. 2011; 5: e1333
        • McAuley J.
        • Boyer K.M.
        • Patel D.
        • Mets M.
        • Swisher C.
        • Roizen N.
        • et al.
        Early and longitudinal evaluations of treated infants and children and untreated historical patients with congenital toxoplasmosis: the Chicago Collaborative Treatment Trial.
        Clin Infect Dis. 1994; 18: 38-72
        • Roizen N.
        • Swisher C.N.
        • Stein M.A.
        • Hopkins J.
        • Boyer K.M.
        • Holfels E.
        • et al.
        Neurologic and developmental outcome in treated congenital toxoplasmosis.
        Pediatrics. 1995; 95: 11-20
        • McLeod R.
        • Boyer K.
        • Karrison T.
        • Kasza K.
        • Swisher C.
        • Roizen N.
        • et al.
        Outcome of treatment for congenital toxoplasmosis, 1981–2004: the National Collaborative Chicago-Based, Congenital Toxoplasmosis Study.
        Clin Infect Dis. 2006; 42: 1383-1394
        • Olariu T.R.
        • Remington J.S.
        • McLeod R.
        • Alam A.
        • Montoya J.G.
        Severe congenital toxoplasmosis in the United States: clinical and serologic findings in untreated infants.
        Pediatr Infect Dis J. 2011; 30: 1056-1061
        • Wilson C.B.
        • Remington J.S.
        • Stagno S.
        • Reynolds D.W.
        Development of adverse sequelae in children born with subclinical congenital Toxoplasma infection.
        Pediatrics. 1980; 66: 767-774
        • Phan L.
        • Kasza K.
        • Jalbrzikowski J.
        • Noble A.G.
        • Latkany P.
        • Kuo A.
        • et al.
        Longitudinal study of new eye lesions in children with toxoplasmosis who were not treated during the first year of life.
        Am J Ophthalmol. 2008; 146: 375-384
        • McLeod R.
        • Boyer K.M.
        • Lee D.
        • Mui E.
        • Wroblewski K.
        • Karrison T.
        • et al.
        Prematurity and severity are associated with Toxoplasma gondii alleles (NCCCTS, 1981–2009).
        Clin Infect Dis. 2012; 54: 1595-1605
        • Wallon M.
        • Kodjikian L.
        • Binquet C.
        • Garweg J.
        • Fleury J.
        • Quantin C.
        • et al.
        Long-term ocular prognosis in 327 children with congenital toxoplasmosis.
        Pediatrics. 2004; 113: 1567-1572
        • Faucher B.
        • Garcia-Meric P.
        • Franck J.
        • Minodier P.
        • Francois P.
        • Gonnet S.
        • et al.
        Long-term ocular outcome in congenital toxoplasmosis: a prospective cohort of treated children.
        J Infect. 2012; 64: 104-109
        • Freeman K.
        • Tan H.K.
        • Prusa A.
        • Petersen E.
        • Buffolano W.
        • Malm G.
        • et al.
        Predictors of retinochoroiditis in children with congenital toxoplasmosis: European, prospective cohort study.
        Pediatrics. 2008; 121: e1215-e1222
        • Sauer A.
        • de la Torre A.
        • Gomez-Marin J.
        • Bourcier T.
        • Garweg J.
        • Speeg-Schatz C.
        • et al.
        Prevention of retinochoroiditis in congenital toxoplasmosis: Europe versus South America.
        Pediatr Infect Dis J. 2011; 30: 601-603