Skip to main content

Advertisement

SpringerLink
Log in

Toxoplasma infection in individuals in central Italy: does a gender-linked risk exist?

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

An accurate estimate of the impact of toxoplasmosis on the population in Italy is not available. We performed a cross-sectional study on individuals living in Italy to assess: (1) differences in access to Toxo testing and in the prevalence of recent and past Toxoplasma gondii infection according to gender and age, and (2) the clinical impact of disease burden on the male patient subset. Reason for testing, condition of in- or outpatient and clinical data were analysed. Between-gender differences were observed in access to the test. Immunoglobulin M (IgM) prevalence was increased in males in the age range 5–34 years [odds ratio (OR) = 2.03, 95% confidence interval (CI) 1.18–3.49, p = 0.01), with a peak at 25–34 years. In females, it decreased in the age range 20–39 years (OR = 0.49, 95% CI 0.32–0.74, p = 0.0008). The attack rate of recent infection was twice as high for males than for females. Estimates pointed out 3.3 and 1.7 events in 1000 at-risk person-years in the male and female cohorts, respectively. Most IgM-positive subjects did not experience severe forms of toxoplasmosis, with 35% having lymphadenopathy. Chorioretinitis, systemic and neurological manifestations were also observed. Our findings suggest that the acute phase of toxoplasmosis is largely unapparent or clinically mild in this area. It is also possible that the disease burden for Toxoplasma infection in Italy is underestimated. Further study should focus on information acquisition and Toxo test access in hospital units for a better estimation of the real burden of mild and severe forms of the disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Jones JL, Kruszon-Moran D, Sanders-Lewis K, Wilson M (2007) Toxoplasma gondii infection in the United States, 1999–2004, decline from the prior decade. Am J Trop Med Hyg 77(3):405–410

    PubMed  Google Scholar 

  2. Hofhuis A, van Pelt W, van Duynhoven YT, Nijhuis CD, Mollema L, van der Klis FR, Havelaar AH, Kortbeek LM (2011) Decreased prevalence and age-specific risk factors for Toxoplasma gondii IgG antibodies in The Netherlands between 1995/1996 and 2006/2007. Epidemiol Infect 139(4):530–538. doi:10.1017/S0950268810001044

    Article  CAS  PubMed  Google Scholar 

  3. Montoya JG, Liesenfeld O (2004) Toxoplasmosis. Lancet 363(9425):1965–1976

    Article  CAS  PubMed  Google Scholar 

  4. Colombo FA, Vidal JE, Penalva de Oliveira AC, Hernandez AV, Bonasser-Filho F, Nogueira RS, Focaccia R, Pereira-Chioccola VL (2005) Diagnosis of cerebral toxoplasmosis in AIDS patients in Brazil: importance of molecular and immunological methods using peripheral blood samples. J Clin Microbiol 43:5044–5047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Liapis K, Baltadakis I, Balotis K, Karakasis D (2010) Multisystem febrile illness in a cord-blood transplant recipient. Clin Infect Dis 51(6):716–717. doi:10.1086/655896, 749–50

    Article  PubMed  Google Scholar 

  6. Hadem J, Schröder F, Winkler T, Gohrbandt B, Fischer D, Korte T, Drexler H (2006) One day from dyspnea to death—unsuccessful application of extracorporeal membrane oxygenation in Toxoplasma myocarditis following bone marrow transplantation. Clin Res Cardiol 95(9):477–481. doi:10.1007/s00392-006-0402-y

    Article  CAS  PubMed  Google Scholar 

  7. Martina MN, Cervera C, Esforzado N, Linares L, Torregrosa V, Sanclemente G, Hoyo I, Cofan F, Oppenheimer F, Miro JM, Campistol JM, Moreno A (2011) Toxoplasma gondii primary infection in renal transplant recipients. Two case reports and literature review. Transpl Int 24:e6–e12. doi:10.1111/j.1432-2277.2010.01173.x

    Article  PubMed  Google Scholar 

  8. Hazan A, Patel RM, Levinson D, Mian U, Gritz DC (2013) A typical bilateral Toxoplasma retinochoroiditis in a bone marrow transplant patient with negative serum titers. J Ophthalmic Inflamm Infect 3(1):23. doi:10.1186/1869-5760-3-23

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fabiani S, Bruschi F (2014) Rheumatological patients undergoing immunosuppressive treatments and parasitic diseases: a review of the literature of clinical cases and perspectives to screen and follow-up active and latent chronic infections. Clin Exp Rheumatol 32:587–596

    PubMed  Google Scholar 

  10. Del Grande C, Contini C, Schiavi E, Rutigliano G, Maritati M, Seraceni S, Pinto B, Dell’Osso L, Bruschi F (2016) Bipolar disorder with psychotic features and ocular toxoplasmosis: a possible pathogenetic role of the parasite? J Nerv Ment Dis (in press)

  11. Fabiani S, Pinto B, Bruschi F (2013) Toxoplasmosis and neuropsychiatric diseases: can serological studies establish a clear relationship? Neurol Sci 34(4):417–425. doi:10.1007/s10072-012-1197-4

    Article  PubMed  Google Scholar 

  12. Flegr J (2013) Influence of latent Toxoplasma infection on human personality, physiology and morphology: pros and cons of the Toxoplasma-human model in studying the manipulation hypothesis. J Exp Biol 216(Pt 1):127–133. doi:10.1242/jeb.073635

    Article  PubMed  Google Scholar 

  13. Galván-Ramírez Mde L, Sánchez-Orozco LV, Rodríguez LR, Rodríguez S, Roig-Melo E, Troyo Sanromán R, Chiquete E, Armendáriz-Borunda J (2013) Seroepidemiology of Toxoplasma gondii infection in drivers involved in road traffic accidents in the metropolitan area of Guadalajara, Jalisco, Mexico. Parasit Vectors 6(1):294. doi:10.1186/1756-3305-6-294

    Article  PubMed Central  Google Scholar 

  14. Hinze-Selch D, Däubener W, Eggert L, Erdag S, Stoltenberg R, Wilms S (2007) A controlled prospective study of Toxoplasma gondii infection in individuals with schizophrenia: beyond seroprevalence. Schizophr Bull 33(3):782–788

    Article  PubMed  PubMed Central  Google Scholar 

  15. Pappas G, Roussos N, Falagas ME (2009) Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol 39(12):1385–1394. doi:10.1016/j.ijpara.2009.04.003

    Article  PubMed  Google Scholar 

  16. Petersen E, Kijlstra A, Stanford M (2012) Epidemiology of ocular toxoplasmosis. Ocul Immunol Inflamm 20(2):68–75. doi:10.3109/09273948.2012.661115

    Article  PubMed  Google Scholar 

  17. Dubey JP (2010) Toxoplasmosis of animals and humans, 2nd edn. CRC Press, Boca Raton, 313 pp

    Google Scholar 

  18. Mosti M, Pinto B, Giromella A, Fabiani S, Cristofani R, Panichi M, Bruschi F (2013) A 4-year evaluation of toxoplasmosis seroprevalence in the general population and in women of reproductive age in central Italy. Epidemiol Infect 141(10):2192–2195. doi:10.1017/S0950268812002841

    Article  CAS  PubMed  Google Scholar 

  19. Moschen ME, Stroffolini T, Arista S, Pistoia D, Giammanco A, Azara A, De Mattia D, Chiaramonte M, Rigo G, Scarpa B (1991) Prevalence of Toxoplasma gondii antibodies among children and teenagers in Italy. Microbiologica 14(3):229–234

    CAS  PubMed  Google Scholar 

  20. Xiao Y, Yin J, Jiang N, Xiang M, Hao L, Lu H, Sang H, Liu X, Xu H, Ankarklev J, Lindh J, Chen Q (2010) Seroepidemiology of human Toxoplasma gondii infection in China. BMC Infect Dis 10:4. doi:10.1186/1471-2334-10-4

    Article  PubMed  PubMed Central  Google Scholar 

  21. Bellali H, Pelloux H, Villena I, Fricker-Hidalgo H, Le Strat Y, Goulet V (2013) Prevalence of toxoplasmosis in France in 1998: is there a difference between men and women? At what age do children become infected? Rev Epidemiol Sante Publique 61(4):311–317. doi:10.1016/j.respe.2012.11.005

    Article  CAS  PubMed  Google Scholar 

  22. Pinto B, Castagna B, Mattei R, Bruzzi R, Chiumiento L, Cristofani R, Buffolano W, Bruschi F (2012) Seroprevalence for toxoplasmosis in individuals living in north west Tuscany: access to Toxo-test in central Italy. Eur J Clin Microbiol Infect Dis 31(6):1151–1156. doi:10.1007/s10096-011-1422-8

    Article  CAS  PubMed  Google Scholar 

  23. Italian Institute for Statistics (2013) Home page at: http://www.istat.it/it/archivio/demografia

  24. Italian Institute for Statistics (2010) Agricultural census. Available online at: http://www.istat.it/it/censimento-agricoltura/agricoltura-2010

  25. Akanmu AS, Osunkalu VO, Ofomah JN, Olowoselu FO (2010) Pattern of demographic risk factors in the seroprevalence of anti-Toxoplasma gondii antibodies in HIV infected patients at the Lagos University Teaching Hospital. Nig Q J Hosp Med 20(1):1–4

    Article  CAS  PubMed  Google Scholar 

  26. Alvarado-Esquivel C, Liesenfeld O, Estrada-Martínez S, Félix-Huerta J (2011) Toxoplasma gondii infection in workers occupationally exposed to raw meat. Occup Med (Lond) 61(4):265–269. doi:10.1093/occmed/kqr032

    Article  CAS  Google Scholar 

  27. Wilking H, Thamm M, Stark K, Aebischer T, Seeber F (2016) Prevalence, incidence estimations, and risk factors of Toxoplasma gondii infection in Germany: a representative, cross-sectional, serological study. Sci Rep 6:22551. doi:10.1038/srep22551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Jones JL, Kruszon-Moran D, Rivera HN, Price C, Wilkins PP (2014) Toxoplasma gondii seroprevalence in the United States 2009–2010 and comparison with the past two decades. Am J Trop Med Hyg 90(6):1135–1139. doi:10.4269/ajtmh.14-0013

    Article  PubMed  PubMed Central  Google Scholar 

  29. Jones JL, Roberts JM (2012) Toxoplasmosis hospitalizations in the United States, 2008, and trends, 1993–2008. Clin Infect Dis 54:e58–e61. doi:10.1093/cid/cir990

    Article  PubMed  Google Scholar 

  30. Bénard A, Petersen E, Salamon R, Chêne G, Gilbert R, Salmi LR; European Toxo Prevention Study Group (EUROTOXO) (2008) Survey of European programmes for the epidemiological surveillance of congenital toxoplasmosis. Euro Surveill 13(15). pii: 18834

  31. Stagni L, Romano MA, Romano A, Magli A, Briganti F, Del Pezzo MA, Buffolano W (2009) Prenatal screening for congenital toxoplasmosis in Campania: preliminary report on activities and results. Mem Inst Oswaldo Cruz 104(2):374–377

    Article  CAS  PubMed  Google Scholar 

  32. Cong W, Liu GH, Meng QF, Dong W, Qin SY, Zhang FK, Zhang XY, Wang XY, Qian AD, Zhu XQ (2015) Toxoplasma gondii infection in cancer patients: prevalence, risk factors, genotypes and association with clinical diagnosis. Cancer Lett 359(2):307–313. doi:10.1016/j.canlet.2015.01.036

    Article  CAS  PubMed  Google Scholar 

  33. Hamza H, El-Taweel H, Abou-Holw S, Khalil S, Wagdy E (2015) Toxoplasma gondii seropositivity in renal patients: rate, pattern, predictors and related morbidity. J Egypt Soc Parasitol 45(1):7–15

    Article  PubMed  Google Scholar 

  34. Wang S, Lan C, Zhang L, Zhang H, Yao Z, Wang D, Ma J, Deng J, Liu S (2015) Seroprevalence of Toxoplasma gondii infection among patients with hand, foot and mouth disease in Henan, China: a hospital-based study. Infect Dis Poverty 4:53. doi:10.1186/s40249-015-0088-3

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Dr. Fioravante Pisaturo of the University Hospital of Pisa for data collecting. We thank Daniele Benvenuti of the University Hospital of Pisa for his help in the diagnosis of hospital discharge cards (DRG) for inpatients.

Author information

Authors and Affiliations

  1. Department of Translational Research, New Technologies in Medicine and Surgery (NTMS), Università di Pisa, via Roma, 55-56126, Pisa, Italy

    B. Pinto & F. Bruschi

  2. Chemical, Clinical and Microbiological Laboratory, USL Toscana Nord Ovest, Lucca, Italy

    R. Mattei

  3. Department of Laboratory Medicine, Pisa University Cisanello Hospital, Pisa, Italy

    G. A. Moscato

  4. Medical Direction, Azienda Ospedaliero, Universitaria Pisana, Pisa, Italy

    M. Cristofano & M. Giraldi

  5. Unit of Genetic & Microbiology, Department of Biology, Università di Pisa, Pisa, Italy

    R. Scarpato

  6. Department of Pediatrics, University Hospital Federico II, Naples, Italy

    W. Buffolano

Authors
  1. B. Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Mattei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. A. Moscato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Cristofano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Giraldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. Scarpato
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. W. Buffolano
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. F. Bruschi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. Pinto.

Ethics declarations

Funding source

None.

Conflict of interest

The authors have no conflicts of interests to declare in relation to this study or publication of its findings.

Ethical approval

The study was approved by the Ethics Committee of the University of Pisa (study 3527).

Informed consent

For this type of study, formal consent is not required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pinto, B., Mattei, R., Moscato, G.A. et al. Toxoplasma infection in individuals in central Italy: does a gender-linked risk exist?. Eur J Clin Microbiol Infect Dis 36, 739–746 (2017). https://doi.org/10.1007/s10096-016-2857-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-016-2857-8

Keywords

Search

Navigation