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Abstract

Background

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.

Aim

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 infection.

Methods

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.

Results

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.

Conclusion

Higher prevalences in older women may reflect a higher past risk of exposure while persistent geographical differences may reflect dietary or environmental differences. 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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2021-02-04
2024-12-21
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References

  1. 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 
  2. 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 
  3. 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 
  4. 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 
  5. 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 
  6. 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 
  7. 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 
  8. 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
  9. 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 
  10. 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 
  11. 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
  12. 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 
  13. 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
  14. 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
  15. Desmonts G, Couvreur J, Ben Rachid MS. [Toxoplasmosis, the mother and the child]. Arch Fr Pediatr. 1965;22(10):1183-200. PMID: 5853819 
  16. 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 
  17. 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
  18. 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
  19. 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 
  20. 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
  21. 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 
  22. 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 
  23. 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 
  24. 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 
  25. 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 
  26. 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 
  27. 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 
  28. 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 
  29. 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/
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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 
  35. 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 
  36. 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/.
  37. 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
  38. 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 
  39. 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 
  40. 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 
  41. 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 
  42. 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
  43. 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
  44. 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 
  45. 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 
  46. 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 
  47. 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 
  48. 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 
  49. 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 
  50. 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 
  51. 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 
  52. 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.
  53. 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 
  54. 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
National perinatal survey demonstrates a decreasing seroprevalence of Toxoplasma gondii infection among pregnant women in France, 1995 to 2016: impact for screening policy
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Eve+Robinson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Robinson Eve</a>, <a href="/search?value1=Henriette+de+Valk&option1=author&noRedirect=true" class="nonDisambigAuthorLink">de Valk Henriette</a>, <a href="/search?value1=Isabelle+Villena&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Villena Isabelle</a>, <a href="/search?value1=Yann+Le+Strat&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Le Strat Yann</a>, <a href="/search?value1=Mathieu+Tourdjman&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tourdjman Mathieu</a></span>. National perinatal survey demonstrates a decreasing seroprevalence of Toxoplasma gondii infection among pregnant women in France, 1995 to 2016: impact for screening policy. <a href="/content/ecdc">Euro Surveill.</a> 2021;26(5):pii=1900710. <a href="https://doi.org/10.2807/1560-7917.ES.2021.26.5.1900710" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2021.26.5.1900710</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 19 Nov 2019;&nbsp;&nbsp; <span class="generated">Accepted</span>: 13 Jul 2020 </span> </p>
/content/10.2807/1560-7917.ES.2021.26.5.1900710
/content/10.2807/1560-7917.ES.2021.26.5.1900710
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