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National perinatal survey demonstrates a decreasing seroprevalence of Toxoplasma gondii infection among pregnant women in France, 1995 to 2016: impact for screening policy
- Eve Robinson1,2 , Henriette de Valk1 , Isabelle Villena3 , Yann Le Strat1 , Mathieu Tourdjman1
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View Affiliations Hide AffiliationsAffiliations: 1 French National Public Health Agency (Santé publique France), Saint-Maurice, France 2 European Programme for Intervention Epidemiology Training (EPIET), European Centre for Disease Prevention and Control (ECDC), Stockholm, Sweden 3 National Reference Centre for Toxoplasmosis, Maison Blanche Hospital, University Reims Champagne-Ardenne, FranceEve Robinsoneveprobinson gmail.com
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Citation style for this article: Robinson Eve, de Valk Henriette, Villena Isabelle, Le Strat Yann, Tourdjman Mathieu. National perinatal survey demonstrates a decreasing seroprevalence of Toxoplasma gondii infection among pregnant women in France, 1995 to 2016: impact for screening policy. Euro Surveill. 2021;26(5):pii=1900710. https://doi.org/10.2807/1560-7917.ES.2021.26.5.1900710 Received: 19 Nov 2019; Accepted: 13 Jul 2020
Abstract
Toxoplasmosis during pregnancy can result in congenital anomalies or fetal death. Universal antenatal screening is recommended in France, a strategy in place since the 1970s.
We determined the seroprevalence of toxoplasmosis among pregnant women participating in the 2016 national perinatal survey (ENP), compared results with previous ENPs, and investigated factors associated with Toxoplasma gondii infection.
Using the 2016 ENP data, which contain sociodemographic and clinical information from all women giving birth during a one week period, we calculated adjusted prevalence ratios (aPR) by sociodemographic factors. Using available data from prior ENPs (1995, 2003 and 2010), we calculated age-standardised seroprevalences and aPRs for French women.
In 2016, seroprevalence was 31.3% overall. Among French women, associations with increasing age (aPR: 1.54; 95% CI: 1.39–1.70), residence in Paris (aPR: 1.19; 95% CI: 1.08–1.31) or south-western regions (aPR: 1.19; 95% CI: 1.08–1.31), and higher professional status (aPR: 1.12; 95%CI 1.04–1.21) were observed. An association with increasing age was also evident among women from North Africa and sub-Saharan Africa. Age-standardised seroprevalence decreased from 55.0% in 1995 to 33.7% in 2016. Among French women, significant associations with age, Paris and south-west regions persisted across all ENPs.
Higher prevalences in older women may reflect a higher past risk of exposure while persistent geographical differences may reflect dietary or environmental differences. Toxoplasma seroprevalence among pregnant women continues to fall and will impact screening effectiveness. This warrants a comprehensive review to determine the appropriate future of prevention in France.
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References
-
Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, et al. , European Research Network on Congenital Toxoplasmosis. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. BMJ. 2000;321(7254):142-7. https://doi.org/10.1136/bmj.321.7254.142 PMID: 10894691
-
Hill D, Dubey JP. Toxoplasma gondii: transmission, diagnosis and prevention. Clin Microbiol Infect. 2002;8(10):634-40. https://doi.org/10.1046/j.1469-0691.2002.00485.x PMID: 12390281
-
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(11):4037-44. https://doi.org/10.1128/JCM.40.11.4037-4044.2002 PMID: 12409371
-
Havelaar AH, Haagsma JA, Mangen MJ, Kemmeren JM, Verhoef LP, Vijgen SM, et al. Disease burden of foodborne pathogens in the Netherlands, 2009. Int J Food Microbiol. 2012;156(3):231-8. https://doi.org/10.1016/j.ijfoodmicro.2012.03.029 PMID: 22541392
-
Mangen MJ, Bouwknegt M, Friesema IH, Haagsma JA, Kortbeek LM, Tariq L, et al. Cost-of-illness and disease burden of food-related pathogens in the Netherlands, 2011. Int J Food Microbiol. 2015;196:84-93. https://doi.org/10.1016/j.ijfoodmicro.2014.11.022 PMID: 25528537
-
Torgerson PR, Devleesschauwer B, Praet N, Speybroeck N, Willingham AL, Kasuga F, et al. World Health Organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: A data synthesis. PLoS Med. 2015;12(12):e1001920. https://doi.org/10.1371/journal.pmed.1001920 PMID: 26633705
-
Batz MB, Hoffmann S, Morris JG Jr. Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J Food Prot. 2012;75(7):1278-91. https://doi.org/10.4315/0362-028X.JFP-11-418 PMID: 22980012
-
World Health Organization (WHO). WHO estimates of the global burden of foodborne diseases Foodborne diseases burden epidemiology reference group 2007-2015. Geneva: WHO; 2015. Available from: https://apps.who.int/iris/bitstream/handle/10665/199350/9789241565165_eng.pdf?sequence=1&isAllowed=y
-
Li XL, Wei HX, Zhang H, Peng HJ, Lindsay DS. A meta analysis on risks of adverse pregnancy outcomes in Toxoplasma gondii infection. PLoS One. 2014;9(5):e97775. https://doi.org/10.1371/journal.pone.0097775 PMID: 24830795
-
Bénard A, Petersen E, Salamon R, Chêne G, Gilbert R, Salmi LR, European Toxo Prevention Study Group (EUROTOXO). Survey of European programmes for the epidemiological surveillance of congenital toxoplasmosis. Euro Surveill. 2008;13(15):18834. https://doi.org/10.2807/ese.13.15.18834-en PMID: 18445459
-
European Centre for Disease Prevention and Control (ECDC). Congenital toxoplasmosis. Annual epidemiological report for 2015. Stockholm: ECDC; 2018. Available from: https://www.ecdc.europa.eu/en/publications-data/congenital-toxoplasmosis-annual-epidemiological-report-2015
-
Villena I, Ancelle T, Delmas C, Garcia P, Brezin AP, Thulliez P, et al. , Toxosurv network and National Reference Centre for Toxoplasmosis. Congenital toxoplasmosis in France in 2007: first results from a national surveillance system. Euro Surveill. 2010;15(25):19600. https://doi.org/10.2807/ese.15.25.19600-en PMID: 20587361
-
King L, Villena I, Ancelle T, Wallon M, Garcia P, Thulliez P, et al. La toxoplasmose congénitale: mise en place d’un dispositif de surveillance en France. [Congenital toxoplasmosis: implementation of a surveillance system in France]. Bull Epidemiol Hebd.2008;14-15:122-24. French. Available from: http://beh.santepubliquefrance.fr/beh/2008/14_15/beh_14_15_2008.pdf
-
National Reference Centre for Toxoplasmosis, Reims University Hospital. (CHU de Reims). Toxoplasmosis monitoring. Reims: Reims University Hospital. [Accessed: 17 May 2020]. Available from: http://cnrtoxoplasmose.chu-reims.fr/?page_id=246&lang=en
-
Desmonts G, Couvreur J, Ben Rachid MS. [Toxoplasmosis, the mother and the child]. Arch Fr Pediatr. 1965;22(10):1183-200. PMID: 5853819
-
Nogareda F, Le Strat Y, Villena I, De Valk H, Goulet V. Incidence and prevalence of Toxoplasma gondii infection in women in France, 1980-2020: model-based estimation. Epidemiol Infect. 2014;142(8):1661-70. https://doi.org/10.1017/S0950268813002756 PMID: 24229712
-
Tourdjman M, Tchéandjieu C, De Valk H, Goulet V, Le Strat Y. Toxoplasmose chez les femmes enceintes en France: évolution de la séroprévalence et des facteurs associés entre 1995 et 2010, à partir des enquêtes nationales périnatales. [Toxoplasmosis among pregnant women in France: trends in seroprevalence and associated factors between 1995 and 2010]. Bull Epidemiol Hebd. 2015;15-16:9. French. Available from: http://beh.santepubliquefrance.fr/beh/2015/15-16/pdf/2015_15-16_5.pdf
-
L’Institut national de la santé et de la recherche médicale (INSERM), La Direction de la recherche dé, de l’évaluation et des statistiques (DREES). Enquête nationale périnatale: Rapport 2016. [National perinatal survey: 2016 Report]. Paris: Ministère des Solidarités et de la Santé; 2017. French. Available from: http://www.xn--epop-inserm-ebb.fr/wp-content/uploads/2017/10/ENP2016_rapport_complet.pdf
-
Berger F, Goulet V, Le Strat Y, Desenclos JC. Toxoplasmosis among pregnant women in France: risk factors and change of prevalence between 1995 and 2003. Rev Epidemiol Sante Publique. 2009;57(4):241-8. https://doi.org/10.1016/j.respe.2009.03.006 PMID: 19577390
-
Institue national de la statistique et des études économiques (INSEE). Zone d'études et d'aménagement du territoire / ZEAT. [Study and regional planning zone/ ZEAT.]. Paris: INSEE. [Accessed: 17 May 2020]. French. Available from: https://www.insee.fr/fr/metadonnees/definition/c1910
-
Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol. 2004;159(7):702-6. https://doi.org/10.1093/aje/kwh090 PMID: 15033648
-
Guigue N, Léon L, Hamane S, Gits-Muselli M, Le Strat Y, Alanio A, et al. Continuous decline of Toxoplasma gondii seroprevalence in hospital: A 1997-2014 longitudinal study in Paris, France. Front Microbiol. 2018;9:2369. https://doi.org/10.3389/fmicb.2018.02369 PMID: 30344515
-
Bigna JJ, Tochie JN, Tounouga DN, Bekolo AO, Ymele NS, Youda EL, et al. Global, regional, and country seroprevalence of Toxoplasma gondii in pregnant women: a systematic review, modelling and meta-analysis. Sci Rep. 2020;10(1):12102. https://doi.org/10.1038/s41598-020-69078-9 PMID: 32694844
-
Jones JL, Kruszon-Moran D, Rivera HN, Price C, Wilkins PP. Toxoplasma gondii seroprevalence in the United States 2009-2010 and comparison with the past two decades. Am J Trop Med Hyg. 2014;90(6):1135-9. https://doi.org/10.4269/ajtmh.14-0013 PMID: 24710615
-
Hofhuis A, van Pelt W, van Duynhoven YT, Nijhuis CD, Mollema L, van der Klis FR, et al. Decreased prevalence and age-specific risk factors for Toxoplasma gondii IgG antibodies in The Netherlands between 1995/1996 and 2006/2007. Epidemiol Infect. 2011;139(4):530-8. https://doi.org/10.1017/S0950268810001044 PMID: 20492743
-
Gargaté MJ, Ferreira I, Vilares A, Martins S, Cardoso C, Silva S, et al. Toxoplasma gondii seroprevalence in the Portuguese population: comparison of three cross-sectional studies spanning three decades. BMJ Open. 2016;6(10):e011648. https://doi.org/10.1136/bmjopen-2016-011648 PMID: 27707823
-
Berghold C, Herzog SA, Jakse H, Berghold A. Prevalence and incidence of toxoplasmosis: a retrospective analysis of mother-child examinations, Styria, Austria, 1995 to 2012. Euro Surveill. 2016;21(33):30317. https://doi.org/10.2807/1560-7917.ES.2016.21.33.30317 PMID: 27562876
-
Opsteegh M, Kortbeek TM, Havelaar AH, van der Giessen JW. Intervention strategies to reduce human Toxoplasma gondii disease burden. Clin Infect Dis. 2015;60(1):101-7. https://doi.org/10.1093/cid/ciu721 PMID: 25225234
-
Agreste. Animaux de boucherie et volailles de chair : consommation de viande. [Slaughter animals and broilers: meat consumption]. Paris: Ministère de l'agriculture et de l'alimentation. French. Available from: https://agreste.agriculture.gouv.fr/agreste-web/disaron/CONSOVIANDE/detail/
-
FranceAgriMer. Ovine meat industry sheet. Montreuil: FranceAgrimer; 2020. Available from: https://www.franceagrimer.fr/fam/content/download/63285/document/FICHE%20FILIERE%20OVINE%202020_EN.PDF?version=3
-
Agreste. En France, la consommation de viande se modifie fortement entre 1960 et 2018. [In France, meat consumption changed significantly between 1960 and 2018]. Primeur; 2020(4). French. Available from: https://agreste.agriculture.gouv.fr/agreste-web/download/publication/publie/Pri2004/Primeur%202020-4%20ConsoViande.pdf
-
Ancelle T, Goulet V, Tirard-Fleury V, Baril L, Du Mazaubrun C, Thulliez P, et al. La toxoplasmose chez la femme enceinte en France en 1995. Résultats d’une Enquête Nationale Périnatale. [Toxoplasmosis among pregnant women in France in 1995. Results of a national perinatal survey], French. Bull Epidemiol Hebd (Paris). 1996; (51):227-9. Available from: http://beh.santepubliquefrance.fr/beh/1996/9651/index.html
-
Agence nationale de sécurité sanitaire de l’alimentation de l’environnement du travail (ANSES). Étude individuelle nationale des consommations alimentaires 3 (INCA 3). Avis de l’Anses Rapport d’expertise collective. [National individual study of food consumption 3 (INCA 3). ANSES opinion; collective expert appraisal report]. Paris: ANSES; 2017. French. Available from: https://www.anses.fr/fr/system/files/NUT2014SA0234Ra.pdf
-
Belluco S, Patuzzi I, Ricci A. Bovine meat versus pork in Toxoplasma gondii transmission in Italy: A quantitative risk assessment model. Int J Food Microbiol. 2018;269:1-11. https://doi.org/10.1016/j.ijfoodmicro.2017.12.026 PMID: 29358131
-
Opsteegh M, Prickaerts S, Frankena K, Evers EG. A quantitative microbial risk assessment for meatborne Toxoplasma gondii infection in The Netherlands. Int J Food Microbiol. 2011;150(2-3):103-14. https://doi.org/10.1016/j.ijfoodmicro.2011.07.022 PMID: 21864927
-
Fédération des Fabricants d’Aliments pour Chiens, Chats, Oiseaux et autres animaux familiers. Les chiffres de la possession animale en France. [Birds and other pets. Figures for animal possession in France]. Paris: FACCO. [Accessed: 28 Jan 2021]. French. Available from: https://www.facco.fr/les-chiffres/.
-
The European Pet Food Industry (FEDIAF). European Facts & Figures 2017. Brussels: FEDIAF. [Accessed: 28 Jan 2021]. Available from: https://fediaf.org/component/attachments/attachments.html?task=attachment&id=2019
-
Flatt A, Shetty N. Seroprevalence and risk factors for toxoplasmosis among antenatal women in London: a re-examination of risk in an ethnically diverse population. Eur J Public Health. 2013;23(4):648-52. https://doi.org/10.1093/eurpub/cks075 PMID: 22696530
-
Bobić B, Villena I, Stillwaggon E. Prevention and mitigation of congenital toxoplasmosis. Economic costs and benefits in diverse settings. Food Waterborne Parasitol. 2019;16:e00058. PMID: 32095628
-
Peyron F, Mc Leod R, Ajzenberg D, Contopoulos-Ioannidis D, Kieffer F, Mandelbrot L, et al. Congenital toxoplasmosis in France and the United States: One parasite, two diverging approaches. PLoS Negl Trop Dis. 2017;11(2):e0005222. https://doi.org/10.1371/journal.pntd.0005222 PMID: 28207736
-
Maldonado YA, Read JS, COMMITTEE ON INFECTIOUS DISEASES. Committee on infectious diseases.Diagnosis, treatment, and prevention of congenital toxoplasmosis in the United States. Pediatrics. 2017;139(2):e20163860. https://doi.org/10.1542/peds.2016-3860 PMID: 28138010
-
Chapple J. Antenatal screening for Toxoplasmosis. External review against criteria set by the UK National Screening Committee. UK National Screening Committee; 2015. Available from: https://legacyscreening.phe.org.uk/policydb_download.php?doc=1141
-
UK National Screening Committee. UK NSC recommendation on antenatal screening for toxoplasmosis. London: Public Health England; Aug 2016. Available from: https://legacyscreening.phe.org.uk/toxoplasmosis
-
Practice bulletin no. 151: Cytomegalovirus, parvovirus B19, varicella zoster, and toxoplasmosis in pregnancy. Obstet Gynecol. 2015;125(6):1510-25. https://doi.org/10.1097/01.AOG.0000466430.19823.53 PMID: 26000539
-
Paquet C, Yudin MH. No. 285-Toxoplasmosis in pregnancy: prevention, screening, and treatment. J Obstet Gynaecol Can. 2018;40(8):e687-93. https://doi.org/10.1016/j.jogc.2018.05.036 PMID: 30103893
-
Di Mario S, Basevi V, Gagliotti C, Spettoli D, Gori G, D’Amico R, et al. Prenatal education for congenital toxoplasmosis. Cochrane Database Syst Rev. 2015; (10):CD006171. PMID: 26493047
-
Gollub EL, Leroy V, Gilbert R, Chêne G, Wallon M, European Toxoprevention Study Group (EUROTOXO). Effectiveness of health education on Toxoplasma-related knowledge, behaviour, and risk of seroconversion in pregnancy. Eur J Obstet Gynecol Reprod Biol. 2008;136(2):137-45. https://doi.org/10.1016/j.ejogrb.2007.09.010 PMID: 17977641
-
Ancelle T, Yera H, Talabani H, Lebuisson A, Thulliez P, Dupouy-Camet J. [How can the cost of screening for toxoplasmosis during pregnancy be reduced?]. Rev Epidemiol Sante Publique. 2009;57(6):411-7. https://doi.org/10.1016/j.respe.2009.08.011 PMID: 19932576
-
Binquet C, Lejeune C, Seror V, Peyron F, Bertaux AC, Scemama O, et al. The cost-effectiveness of neonatal versus prenatal screening for congenital toxoplasmosis. PLoS One. 2019;14(9):e0221709. https://doi.org/10.1371/journal.pone.0221709 PMID: 31532766
-
Prusa AR, Kasper DC, Sawers L, Walter E, Hayde M, Stillwaggon E. Congenital toxoplasmosis in Austria: Prenatal screening for prevention is cost-saving. PLoS Negl Trop Dis. 2017;11(7):e0005648. https://doi.org/10.1371/journal.pntd.0005648 PMID: 28692640
-
Innes EA, Hamilton C, Garcia JL, Chryssafidis A, Smith D. A one health approach to vaccines against Toxoplasma gondii. Food Waterborne Parasitol. 2019;15:e00053. PMID: 32095623
-
European Food Safety Authority. Scientific opinion of the panel on biological hazards on a request from EFSA on surveillance and monitoring of Toxoplasma in humans, foods and animals. EFSA J. 2007; (583):1-64.
-
Djokic V, Blaga R, Aubert D, Durand B, Perret C, Geers R, et al. Toxoplasma gondii infection in pork produced in France. Parasitology. 2016;143(5):557-67. https://doi.org/10.1017/S0031182015001870 PMID: 26928081
-
Agence française de sécurité sanitaire des aliments (AFSSA). Toxoplasmose: état des connaissances et évaluation du risque lié à l’alimentation. Rapport du groupe de travail “Toxoplasma gondii” de l’Afssa. [Toxoplasmosis: knowledge and assessment of the risk associated with food. Report of the Afssa "Toxoplasma gondii" working group]. Paris: AFSSA. Dec 2005. French. Available from: https://www.anses.fr/fr/content/toxoplasmose-%C3%A9tat-des-connaissances-et-%C3%A9valuation-du-risque-li%C3%A9-%C3%A0-l%E2%80%99alimentation-rapport-d-2
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