Skip to main content Accessibility help
×
×
Home

Maternal infection during pregnancy and type 1 diabetes mellitus in offspring: a systematic review and meta-analysis

  • Y. Yue (a1) (a2), Y. Tang (a2), J. Tang (a1) (a2), J. Shi (a1) (a2), T. Zhu (a1) (a2), J. Huang (a1) (a2), X. Qiu (a1) (a2), Y. Zeng (a1) (a2), W. Li (a1) (a2), Y. Qu (a1) (a2) and D. Mu (a1) (a2)...

Abstract

Previous studies have demonstrated that type 1 diabetes mellitus (T1DM) could be triggered by an early childhood infection. Whether maternal infection during pregnancy is associated with T1DM in offspring is unknown. Therefore, we aimed to study the association using a systematic review and meta-analysis. Eighteen studies including 4304 cases and 25 846 participants were enrolled in this meta-analysis. Odds ratios (ORs) and 95% confidence intervals (CIs) were synthesised using random-effects models. Subgroup analyses and sensitivity analyses were conducted to assess the robustness of associations. Overall, the pooled analysis yielded a statistically significant association between maternal infection during pregnancy and childhood T1DM (OR 1.31, 95% CI 1.07–1.62). Furthermore, six studies that tested maternal enterovirus infection showed a pooled OR of 1.54 (95% CI 1.05–2.27). Heterogeneity from different studies was evident (I2 = 70.1%, P < 0.001) and was mainly attributable to the different study designs, ascertaining methods and sample size among different studies. This study provides evidence for an association between maternal infection during pregnancy and childhood T1DM.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Maternal infection during pregnancy and type 1 diabetes mellitus in offspring: a systematic review and meta-analysis
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Maternal infection during pregnancy and type 1 diabetes mellitus in offspring: a systematic review and meta-analysis
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Maternal infection during pregnancy and type 1 diabetes mellitus in offspring: a systematic review and meta-analysis
      Available formats
      ×

Copyright

Corresponding author

Author for correspondence: D. Mu, E-mail: mudz@scu.edu.cn

Footnotes

Hide All
*

These authors contributed equally to this report.

Footnotes

References

Hide All
1.Skrodeniene, E et al. (2008) Environmental risk factors in prediction of childhood prediabetes. Medicina 44, 5663.
2.Daneman, D (2006) Type 1 diabetes. The Lancet 367, 847858.
3.Narayan, KM et al. (2003) Lifetime risk for diabetes mellitus in the United States. Jama 290, 18841890.
4.Zinkernagel, RM (2001) Maternal antibodies, childhood infections, and autoimmune diseases. New England Journal of Medicine 345, 13311335.
5.Hermann, E et al. (2002) Human fetuses are able to mount an adultlike CD8T-cell response. Blood 100, 21532158.
6.Goldman, M and Marchant, A (2003) The impact of maternal infection or immunization on early-onset autoimmune diabetes. Vaccine 21, 34223425.
7.Wells, GA et al. (2011) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analysis. Available at http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (Accessed 4 June 2018).
8.Otonkoski, T et al. (2000) Neonatal Type I diabetes associated with maternal echovirus 6 infection: a case report. Diabetologia 43, 12351238.
9.Lönnrot, M et al. (1998) Onset of type 1 diabetes mellitus in infancy after enterovirus infections. Diabetic Medicine 15, 431434.
10.Dahlquist, GG, Boman, JE and Juto, P (1999) Enteroviral RNA and IgM antibodies in early pregnancy and risk for childhood-onset IDDM in offspring. Diabetes Care 22, 364365.
11.Lernmark, A et al. (2015) Factors affecting the risk for the first appearance of an islet autoantibody in The Environmental Determinants of Diabetes in the Young (TEDDY). Diabetologia 58, S22.
12.Ali, B et al. (2016) Assessment of environmental factors and the risk of type 1 diabetes in children in Minia Governorate, Egypt; case-control study. Pediatric Diabetes 17, 112.
13.Ludvigsson, J and Wahlberg, J (2002) Diabetes-related autoantibodies in cord blood from children of healthy mothers have disappeared by the time the child is one year old. Annals of the New York Academy of Sciences 958, 289292.
14.Lönnrot, M et al. (2000) Enterovirus infection as a risk factor for beta-cell autoimmunity in a prospectively observed birth cohort: the Finnish diabetes prediction and prevention study. Diabetes 49, 13141318.
15.Hyöty, H et al. (1995) A prospective study of the role of coxsackie B and other enterovirus infections in the pathogenesis of IDDM. Diabetes 44, 652657.
16.Dahlquist, G et al. (1995) Indications that maternal coxsackie B virus infection during pregnancy is a risk factor for childhood-onset IDDM. Diabetologia 38, 13711373.
17.Elfving, M et al. (2008) Maternal enterovirus infection during pregnancy as a risk factor in offspring diagnosed with type 1 diabetes between 15 and 30 years of age. Experimental Diabetes Research 2008, 271958.
18.Sadeharju, K et al. (2001) Enterovirus antibody levels during the first two years of life in prediabetic autoantibody-positive children. Diabetologia 44, 818823.
19.Hiltunen, M et al. (1995) Serological evaluation of the role of cytomegalovirus in the pathogenesis of IDDM: a prospective study. Diabetologia 38, 705710.
20.Blom, L et al. (1989) The Swedish childhood diabetes study – social and perinatal determinants for diabetes in childhood. Diabetologia 32, 713.
21.Dahlquist, GG et al. (1995) Maternal enteroviral infection during pregnancy as a risk factor for childhood IDDM: a population-based case-control study. Diabetes 44, 408413.
22.Viskari, HR et al. (2002) Maternal first-trimester enterovirus infection and future risk of type 1 diabetes in the exposed fetus. Diabetes 51, 25682571.
23.Viskari, H et al. (2012) Maternal enterovirus infection as a risk factor for type 1 diabetes in the exposed offspring. Diabetes care 35, 13281332.
24.Awadalla, NJ et al. (2017) Environmental factors associated with type 1 diabetes development: a case control study in Egypt. International Journal of Environmental Research and Public Health 14, 615.
25.Füchtenbusch, M et al. (2001) 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 17, 333340.
26.Lee, HY et al. (2015) Perinatal and childhood risk factors for early-onset type 1 diabetes: a population-based case-control study in Taiwan. The European Journal of Public Health 25, 10241029.
27.Lynch, KF et al. (2018) Gestational respiratory infections interacting with offspring HLA and CTLA-4 modifies incident beta-cell autoantibodies. Journal of Autoimmunity 86, 93103.
28.Majeed, AAS and Mea, KH (2011) Risk factors for type 1 diabetes mellitus among children and adolescents in Basrah. Oman Medical Journal 26, 189195.
29.Marshall, AL et al. (2004) Type 1 diabetes mellitus in childhood: a matched case control study in Lancashire and Cumbria, UK. Diabetic Medicine 21, 10351040.
30.McKinney, PA et al. (1997) Antenatal risk factors for childhood diabetes mellitus; a case-control study of medical record data in Yorkshire, UK. Diabetologia 40, 933939.
31.EURODIAB Substudy 2 (2000) Infections and vaccinations as risk factors for childhood type I (insulin-dependent) diabetes mellitus: a multicentre case-control investigation. Diabetologia 43, 4753.
32.Sadeharju, K et al. (2003) Enterovirus infections as a risk factor for type I diabetes: virus analyses in a dietary intervention trial. Clinical and Experimental Immunology 132, 271277.
33.Salminen, K et al. (2003) Enterovirus infections are associated with the induction of β-cell autoimmunity in a prospective birth cohort study. Journal of Medical Virology 69, 9198.
34.Šipetić, SB et al. (2005) The Belgrade childhood diabetes study: a multivariate analysis of risk determinants for diabetes. The European Journal of Public Health 15, 117122.
35.Stene, LC et al. (2003) Symptoms of common maternal infections in pregnancy and risk of islet autoimmunity in early childhood. Diabetes Care 26, 31363141.
36.Visalli, N et al. (2003) Environmental risk factors for type 1 diabetes in Rome and province. Archives of Disease in Childhood 88, 695698.
37.Wahlberg, J et al. (2005) Environmental factors related to the induction of beta-cell autoantibodies in 1-yr-old healthy children. Pediatric Diabetes 6, 199205.
38.Ziegler, AG et al. (2013) Seroconversion to multiple islet autoantibodies and risk of progression to diabetes in children. Jama 309, 24732479.
39.Devendra, D, Liu, E and Eisenbarth, GS (2004) Type 1 diabetes: recent developments. British Medical Journal 328, 750754.
40.Maclaren, NK and Atkinson, MA (1997) Insulin-dependent diabetes mellitus: the hypothesis of molecular mimicry between islet cell antigens and microorganisms. Molecular Medicine Today 3, 7683.
41.Ilonen, J et al. (2009) Environmental factors and primary prevention in type 1 diabetes. Pediatric Endocrinology, Diabetes, and Metabolism 15, 227232.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Epidemiology & Infection
  • ISSN: 0950-2688
  • EISSN: 1469-4409
  • URL: /core/journals/epidemiology-and-infection
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
WORD
Supplementary materials

Yue et al. supplementary material
Tables S1-S2 and Figures S1-S8

 Word (324 KB)
324 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed