Experimental Diabetes Research
Volume 2008 (2008), Article ID 271958, 6 pages
doi:10.1155/2008/271958
Research Article

Maternal Enterovirus Infection during Pregnancy as a Risk Factor in Offspring Diagnosed with Type 1 Diabetes between 15 and 30 Years of Age

1Department of Clinical Sciences, Pediatric Unit, Lund University Hospital, Lund University, 221 85 Lund, Sweden
2Department of Clinical Sciences, Pediatric Unit, Malmö University Hospital, Lund University, 205 02 Malmö, Sweden
3Department of Virology, Tampere University Hospital, University of Tampere, 33521 Tampere, Finland
4Department of Women's and Children's Health, Uppsala University, 751 05 Uppsala, Sweden
5Department of Clinical Sciences, Obstetrics and Gynecology Unit, Malmö University Hospital, Lund University, 205 02 Malmö, Sweden
6Department of Clinical Sciences, Diabetes and Celiac Disease Unit, Malmö University Hospital, Lund University, 205 02 Malmö, Sweden
7Department of Medicine, University of Washington, Seattle, WA 98195, USA

Received 10 December 2007; Revised 29 April 2008; Accepted 12 June 2008

Academic Editor: Rodica Pop-Busui

Copyright © 2008 Maria Elfving et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Green and C. C. Patterson, “Trends in the incidence of childhood-onset diabetes in Europe 1989–1998,” Diabetologia, vol. 44, pp. B3–B8, 2001. View at Publisher · View at Google Scholar
  2. E. A. M. Gale, “The rise of childhood type 1 diabetes in the 20th century,” Diabetes, vol. 51, no. 12, pp. 3353–3361, 2002. View at Publisher · View at Google Scholar
  3. A. Pundziute-Lyckå, G. Dahlquist, B. Urbonaite, and R. Žalinkevičius, “Time trend of childhood type 1 diabetes incidence in Lithuania and Sweden, 1983–2000,” Acta Paediatrica, vol. 93, no. 11, pp. 1519–1524, 2004. View at Publisher · View at Google Scholar · View at PubMed
  4. K. Bessaoud, G. Boudraa, M. M. de Ropolo, et al., “Incidence and trends of childhood type 1 diabetes worldwide 1990–1999,” Diabetic Medicine, vol. 23, no. 8, pp. 857–866, 2006. View at Publisher · View at Google Scholar · View at PubMed
  5. L. Nyström, G. Dahlquist, J. Östman, et al., “Risk of developing insulin-dependent diabetes mellitus (IDDM) before 35 years of age: indications of climatological determinants for age at onset,” International Journal of Epidemiology, vol. 21, no. 2, pp. 352–358, 1992. View at Publisher · View at Google Scholar
  6. E. A. M. Gale and K. M. Gillespie, “Diabetes and gender,” Diabetologia, vol. 44, no. 1, pp. 3–15, 2001. View at Publisher · View at Google Scholar
  7. G. Blohmé, L. Nyström, H. J. Arnqvist, et al., “Male predominance of type 1 (insulin-dependent) diabetes mellitus in young adults: results from a 5-year prospective nationwide study of the 15–34-year age group in Sweden,” Diabetologia, vol. 35, no. 1, pp. 56–62, 1992. View at Publisher · View at Google Scholar
  8. G. Dahlquist and B. Källén, “Maternal-child blood group incompatibility and other perinatal events increase the risk for early-onset type 1 (insulin-dependent) diabetes mellitus,” Diabetologia, vol. 35, no. 7, pp. 671–675, 1992. View at Publisher · View at Google Scholar
  9. G. G. Dahlquist, C. Patterson, and G. Soltesz, “Perinatal risk factors for childhood type I diabetes in Europe: the EURODIAB Substudy 2 Study Group,” Diabetes Care, vol. 22, no. 10, pp. 1698–1702, 1999. View at Publisher · View at Google Scholar
  10. P. A. McKinney, R. Parslow, K. A. Gurney, G. R. Law, H. J. Bodansky, and R. Williams, “Perinatal and neonatal determinants of childhood type 1 diabetes. A case-control study in Yorkshire, U.K,” Diabetes Care, vol. 22, no. 6, pp. 928–932, 1999. View at Publisher · View at Google Scholar
  11. M. Elfving, B. Lindberg, M. Landin-Olsson, C. S. Hampe, Å. Lernmark, and S.-A. Ivarsson, “Islet cell autoantibodies in cord blood from children with blood group incompatibility or hyperbilirubinemia,” Autoimmunity, vol. 36, no. 2, pp. 111–115, 2003. View at Publisher · View at Google Scholar
  12. L. C. Stene, K. Barriga, J. M. Norris, et al., “Perinatal factors and development of islet autoimmunity in early childhood. The Diabetes Autoimmunity Study in the Young,” American Journal of Epidemiology, vol. 160, no. 1, pp. 3–10, 2004. View at Publisher · View at Google Scholar · View at PubMed
  13. J. M. Forrest, M. A. Menser, and J. A. Burgess, “High frequency of diabetes mellitus in young adults with congenital rubella,” The Lancet, vol. 289, no. 7720, pp. 332–334, 1971. View at Publisher · View at Google Scholar
  14. M. A. Menser, J. M. Forrest, and R. D. Bransby, “Rubella infection and diabetes mellitus,” The Lancet, vol. 311, no. 8055, pp. 57–60, 1978. View at Publisher · View at Google Scholar
  15. E. D. G. McIntosh and M. A. Menser, “A fifty-year follow-up of congenital rubella,” The Lancet, vol. 340, no. 8816, pp. 414–415, 1992. View at Publisher · View at Google Scholar
  16. E. Barrett-Connor, “Is insulin-dependent diabetes mellitus caused by coxsackie virus B infection? A review of the epidemiologic evidence,” Reviews of Infectious Diseases, vol. 7, no. 2, pp. 207–215, 1985.
  17. M. Roivainen, M. Knip, H. Hyöty, et al., “Several different enterovirus serotypes can be associated with prediabetic autoimmune episodes and onset of overt IDDM. The Childhood Diabetes in Finland (DiMe) Study Group,” Journal of Medical Virology, vol. 56, no. 1, pp. 74–78, 1998. View at Publisher · View at Google Scholar
  18. H. Yin, A.-K. Berg, T. Tuvemo, and G. Frisk, “Enterovirus RNA is found in peripheral blood mononuclear cells in a majority of type 1 diabetic children at onset,” Diabetes, vol. 51, no. 6, pp. 1964–1971, 2002. View at Publisher · View at Google Scholar
  19. H. Hyöty and K. W. Taylor, “The role of viruses in diabetes,” Diabetologia, vol. 45, no. 10, pp. 1353–1361, 2002. View at Publisher · View at Google Scholar · View at PubMed
  20. K. Salminen, K. Sadeharju, M. Lönnrot, et al., “Enterovirus infections are associated with the induction of β-cell autoimmunity in a prospective birth cohort study,” Journal of Medical Virology, vol. 69, no. 1, pp. 91–98, 2003. View at Publisher · View at Google Scholar · View at PubMed
  21. H. Hyöty, M. Hiltunen, M. Knip, et al., “A prospective study of the role of coxsackie B and other enterovirus infections in the pathogenesis of IDDM. The Childhood Diabetes in Finland (DiMe) Study Group,” Diabetes, vol. 44, no. 6, pp. 652–657, 1995. View at Publisher · View at Google Scholar
  22. G. Dahlquist, G. Frisk, S.-A. Ivarsson, L. Svanberg, M. Forsgren, and H. Diderholm, “Indications that maternal coxsackie B virus infection during pregnancy is a risk factor for childhood-onset IDDM,” Diabetologia, vol. 38, no. 11, pp. 1371–1373, 1995. View at Publisher · View at Google Scholar
  23. G. G. Dahlquist, S.-A. Ivarsson, B. Lindberg, and M. Forsgren, “Maternal enteroviral infection during pregnancy as a risk factor for childhood IDDM. A population-based case-control study,” Diabetes, vol. 44, no. 4, pp. 408–413, 1995. View at Publisher · View at Google Scholar
  24. G. G. Dahlquist, J. E. Boman, and P. Juto, “Enteroviral RNA and IgM antibodies in early pregnancy and risk for childhood-onset IDDM in offspring,” Diabetes Care, vol. 22, no. 2, pp. 364–365, 1999. View at Publisher · View at Google Scholar
  25. M. Elfving, B. Lindberg, L. Nyström, G. Sundkvist, Å. Lernmark, and S.-A. Ivarsson, “Islet autoantibodies in cord blood from patients who developed type 1 diabetes mellitus at 15–30 years of age,” Autoimmunity, vol. 36, no. 4, pp. 227–231, 2003. View at Publisher · View at Google Scholar
  26. J. Östman, H. Arnqvist, G. Blohmé, et al., “Epidemiology of diabetes mellitus in Sweden. Results of the first year of a prospective study in the population age group 15–34 years,” Acta Medica Scandinavica, vol. 220, no. 5, pp. 437–445, 1986.
  27. S. Juhela, H. Hyöty, A. Hinkkanen, et al., “T cell responses to enterovirus antigens and to β-cell autoantigens in unaffected children positive for IDDM-associated autoantibodies,” Journal of Autoimmunity, vol. 12, no. 4, pp. 269–278, 1999. View at Publisher · View at Google Scholar · View at PubMed
  28. M. Lönnrot, K. Korpela, M. Knip, et al., “Enterovirus infections as a risk factor for β-cell autoimmunity in a prospectively observed birth cohort: the Finnish Diabetes Prediction and Prevention Study,” Diabetes, vol. 49, no. 8, pp. 1314–1318, 2000. View at Publisher · View at Google Scholar
  29. M. Lönnrot, M. Sjöroos, K. Salminen, M. Maaronen, T. Hyypiä, and H. Hyöty, “Diagnosis of enterovirus and rhinovirus infections by RT-PCR and time-resolved fluorometry with lanthanide chelate labeled probes,” Journal of Medical Virology, vol. 59, no. 3, pp. 378–384, 1999. View at Publisher · View at Google Scholar
  30. H. E. Larsson, K. Lynch, B. Lernmark, et al., “Diabetes-associated HLA genotypes affect birthweight in the general population,” Diabetologia, vol. 48, no. 8, pp. 1484–1491, 2005. View at Publisher · View at Google Scholar · View at PubMed
  31. W. A. Hagopian, Å. Lernmark, M. J. Rewers, et al., “TEDDY–the environmental determinants of diabetes in the young: an observational clinical trial,” Annals of the New York Academy of Sciences, vol. 1079, pp. 320–326, 2006. View at Publisher · View at Google Scholar · View at PubMed
  32. T. Vuorinen, R. Vainionpää, H. Kettinen, and T. Hyypiä, “Coxsackie virus B3 infection in human leukocytes and lymphoid cell lines,” Blood, vol. 84, no. 3, pp. 823–829, 1994.
  33. T. Otonkoski, M. Roivainen, O. Vaarala, et al., “Neonatal type I diabetes associated with maternal echovirus 6 infection: a case report,” Diabetologia, vol. 43, no. 10, pp. 1235–1238, 2000. View at Publisher · View at Google Scholar
  34. H. R. Viskari, M. Roivainen, A. Reunanen, et al., “Maternal first-trimester enterovirus infection and future risk of type 1 diabetes in the exposed fetus,” Diabetes, vol. 51, no. 8, pp. 2568–2571, 2002. View at Publisher · View at Google Scholar
  35. M. Füchtenbusch, A. Irnstetter, G. Jäger, and A.-G. Ziegler, “No evidence for an association of coxsackie virus infections during pregnancy and early childhood with development of islet autoantibodies in offspring of mothers or fathers with type 1 diabetes,” Journal of Autoimmunity, vol. 17, no. 4, pp. 333–340, 2001. View at Publisher · View at Google Scholar · View at PubMed
  36. J. W. Yoon, “The role of viruses and environmental factors in the induction of diabetes,” Current Topics in Microbiology and Immunology, vol. 164, pp. 95–123, 1990.
  37. M. Hiltunen, H. Hyöty, M. Knip, et al., “Islet cell antibody seroconversion in children is temporally associated with enterovirus infections,” Journal of Infectious Diseases, vol. 175, no. 3, pp. 554–560, 1997.
  38. D. M. Morens and M. A. Pallansch, “Epidemiology,” in Human Enterovirus Infections, H. A. Rotbart, Ed., pp. 3–23, ASM Press, Washington, DC, USA, 1995.
  39. K. Sadeharju, M. Knip, M. Hiltunen, H. K. Åkerblom, and H. Hyöty, “The HLA-DR phenotype modulates the humoral immune response to enterovirus antigens,” Diabetologia, vol. 46, no. 8, pp. 1100–1105, 2003. View at Publisher · View at Google Scholar · View at PubMed