Enterovirus infection is associated with an increased risk of childhood type 1 diabetes in Taiwan: a nationwide population-based cohort study

Diabetologia

Volumn 58, Issue 1, 2015, Pages 79-86

  Lin, Hsiao Chuan ^a,b,c   Wang, Chung Hsing ^b,c   Tsai, Fuu Jen ^a,c   Hwang, Kao Pin ^b,c   Chen, Walter ^b,c   Lin, Cheng Chieh ^b,c   Li, Tsai Chung ^a,d  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d ASIA UNIVERSITY   (Taiwan)

Author keywords

Enterovirus; National Health Insurance programme; Type 1 diabetes

Indexed keywords

AGE DISTRIBUTION; ALLERGIC RHINITIS; ARTICLE; ASTHMA; ATOPY; CHILD; CHILDHOOD DISEASE; COHORT ANALYSIS; DATA BASE; DISEASE ASSOCIATION; ENTEROVIRUS INFECTION; FEMALE; HEALTH INSURANCE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; NATIONAL HEALTH INSURANCE; POPULATION RESEARCH; PRESCHOOL CHILD; RISK ASSESSMENT; SCHOOL CHILD; SEX DIFFERENCE; TAIWAN; ADOLESCENT; DIABETES MELLITUS, TYPE 1; ENTEROVIRUS INFECTIONS; FACTUAL DATABASE; INCIDENCE; INFANT; RISK FACTOR;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; DATABASES, FACTUAL; DIABETES MELLITUS, TYPE 1; ENTEROVIRUS INFECTIONS; FEMALE; HUMANS; INCIDENCE; INFANT; MALE; RISK FACTORS; TAIWAN;

EID: 84916640838     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3400-z     Document Type: Article

References (49)

1. EURODIAB ACE Study Group (2000) Variation and trends in incidence of childhood diabetes in Europe. EURODIAB ACE Study Group. Lancet 355:873–876
2. Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G (2009) Incidence trends for childhood type 1 diabetes in Europe during 1989–2003 and predicted new cases 2005–20: a multicentre prospective registration study. Lancet 373:2027–2033
3. Chong JW, Craig ME, Cameron FJ et al (2007) Marked increase in type 1 diabetes mellitus incidence in children aged 0–14 yr in Victoria, Australia, from 1999 to 2002. Pediatr Diabetes 8:67–73
4. The DIAMOND Project Group (2006) Incidence and trends of childhood type 1 diabetes worldwide 1990–1999. Diabet Med 23:857–866
5. Patterson CC, Gyurus E, Rosenbauer J et al (2012) Trends in childhood type 1 diabetes incidence in Europe during 1989–2008: evidence of non-uniformity over time in rates of increase. Diabetologia 55:2142–2147
6. Harjutsalo V, Sund R, Knip M, Groop P-H (2013) Incidence of type 1 diabetes in Finland letters. JAMA 310:427–428
7. Tseng CH (2008) Incidence of type 1 diabetes mellitus in children aged 0–14 years during 1992–1996 in Taiwan. Acta Paediatr 97:392–393
8. Hober D, Sauter P (2010) Pathogenesis of type 1 diabetes mellitus: interplay between enterovirus and host. Nat Rev Endocrinol 6:279–289
9. Tauriainen S, Oikarinen S, Oikarinen M, Hyoty H (2011) Enteroviruses in the pathogenesis of type 1 diabetes. Semin Immunopathol 33:45–55
10. Yeung WC, Rawlinson WD, Craig ME (2011) Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 342:d35
11. Gamble DR, Kinsley ML, FitzGerald MG, Bolton R, Taylor KW (1969) Viral antibodies in diabetes mellitus. Br Med J 3:627–630
12. Gamble DR, Taylor KW (1969) Seasonal incidence of diabetes mellitus. Br Med J 3:631–633
13. Laitinen OH, Honkanen H, Pakkanen O et al (2014) Coxsackievirus B1 is associated with induction of beta-cell autoimmunity that portends type 1 diabetes. Diabetes 63:446–455
14. Oikarinen S, Tauriainen S, Hober D et al (2014) Virus antibody survey in different European populations indicates risk association between coxsackievirus B1 and type 1 diabetes. Diabetes 63:655–662
15. Jaidane H, Hober D (2008) Role of coxsackievirus B4 in the pathogenesis of type 1 diabetes. Diabetes Metab 34:537–548
16. Frisk G, Nilsson E, Tuvemo T, Friman G, Diderholm H (1992) The possible role of Coxsackie A and echo viruses in the pathogenesis of type I diabetes mellitus studied by IgM analysis. J Infect 24:13–22
17. Helfand RF, Gary HE Jr, Freeman CY, Anderson LJ, Pallansch MA (1995) Serologic evidence of an association between enteroviruses and the onset of type 1 diabetes mellitus. Pittsburgh Diabetes Research Group. J Infect Dis 172:1206–1211
18. Roivainen M, Knip M, Hyoty H et al (1998) Several different enterovirus serotypes can be associated with prediabetic autoimmune episodes and onset of overt IDDM. Childhood Diabetes in Finland (DiMe) Study Group. J Med Virol 56:74–78
19. Salvatoni A, Baj A, Bianchi G, Federico G, Colombo M, Toniolo A (2013) Intrafamilial spread of enterovirus infections at the clinical onset of type 1 diabetes. Pediatr Diabetes 14:407–416
20. Gleason RE, Kahn CB, Funk IB, Craighead JE (1982) Seasonal incidence of insulin-dependent diabetes (IDDM) in Massachusetts, 1964–1973. Int J Epidemiol 11:39–45
21. Huff JC, Hierholzer JC, Farris WA (1974) An “outbreak” of juvenile diabetes mellitus: consideration of a viral etiology. Am J Epidemiol 100:277–287
22. Oikarinen S, Martiskainen M, Tauriainen S et al (2011) Enterovirus RNA in blood is linked to the development of type 1 diabetes. Diabetes 60:276–279
23. Richardson SJ, Leete P, Bone AJ, Foulis AK, Morgan NG (2013) Expression of the enteroviral capsid protein VP1 in the islet cells of patients with type 1 diabetes is associated with induction of protein kinase R and downregulation of Mcl-1. Diabetologia 56:185–193
24. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG (2011) Immunohistochemical analysis of the relationship between islet cell proliferation and the production of the enteroviral capsid protein, VP1, in the islets of patients with recent-onset type 1 diabetes. Diabetologia 54:2417–2420
25. Krogvold L, Edwin B, Buanes T et al (2014) Pancreatic biopsy by minimal tail resection in live adult patients at the onset of type 1 diabetes: experiences from the DiViD study. Diabetologia 57:841–843
26. Campbell-Thompson ML, Atkinson MA, Butler AE et al (2013) The diagnosis of insulitis in human type 1 diabetes. Diabetologia 56:2541–2543
27. Oikarinen M, Tauriainen S, Oikarinen S et al (2012) Type 1 diabetes is associated with enterovirus infection in gut mucosa. Diabetes 61:687–691
28. Campbell-Thompson M, Wasserfall C, Kaddis J et al (2012) Network for Pancreatic Organ Donors with Diabetes (nPOD): developing a tissue biobank for type 1 diabetes. Diabetes Metab Res Rev 28:608–617
29. Sarmiento L, Cabrera-Rode E, Lekuleni L et al (2007) Occurrence of enterovirus RNA in serum of children with newly diagnosed type 1 diabetes and islet cell autoantibody-positive subjects in a population with a low incidence of type 1 diabetes. Autoimmunity 40:540–545
30. Craig ME, Howard NJ, Silink M, Rawlinson WD (2003) Reduced frequency of HLA DRB1*03-DQB1*02 in children with type 1 diabetes associated with enterovirus RNA. J Infect Dis 187:1562–1570
31. Maha MM, Ali MA, Abdel-Rehim SE, Abu-Shady EA, El-Naggar BM, Maha YZ (2003) The role of coxsackieviruses infection in the children of insulin dependent diabetes mellitus. J Egypt Public Health Assoc 78:305–318
32. Kawashima H, Ihara T, Ioi H et al (2004) Enterovirus-related type 1 diabetes mellitus and antibodies to glutamic acid decarboxylase in Japan. J Infect 49:147–151
33. Stene LC, Ronningen KS, Bjornvold M, Undlien DE, Joner G (2010) An inverse association between history of childhood eczema and subsequent risk of type 1 diabetes that is not likely to be explained by HLA-DQ, PTPN22, or CTLA4 polymorphisms. Pediatr Diabetes 11:386–393
34. Lu JF, Hsiao WC (2003) Does universal health insurance make health care unaffordable? Lessons from Taiwan. Health Aff (Millwood) 22:77–88
35. Newhook LA, Penney S, Fiander J, Dowden J (2012) Recent incidence of type 1 diabetes mellitus in children 0-14 years in Newfoundland and Labrador, Canada climbs to over 45/100,000: a retrospective time trend study. BMC Res Notes 5:628
36. TEDDY Study Group (2008) The Environmental Determinants of Diabetes in the Young (TEDDY) study. Ann N Y Acad Sci 1150:1–13
37. Viskari H, Ludvigsson J, Uibo R et al (2004) Relationship between the incidence of type 1 diabetes and enterovirus infections in different European populations: results from the EPIVIR project. J Med Virol 72:610–617
38. Noble JA, Erlich HA (2012) Genetics of type 1 diabetes. Cold Spring Harb Perspect Med 2:a007732
39. Stankov K, Benc D, Draskovic D (2013) Genetic and epigenetic factors in etiology of diabetes mellitus type 1. Pediatrics 132:1112–1122
40. Hermann R, Turpeinen H, Laine AP et al (2003) HLA DR-DQ-encoded genetic determinants of childhood-onset type 1 diabetes in Finland: an analysis of 622 nuclear families. Tissue Antigens 62:162–169
41. Pugliese A, Gianani R, Moromisato R et al (1995) HLA-DQB1*0602 is associated with dominant protection from diabetes even among islet cell antibody-positive first-degree relatives of patients with IDDM. Diabetes 44:608–613
42. Sanjeevi CB (2000) HLA-DQ6-mediated protection in IDDM. Hum Immunol 61:148–153
43. Stanescu DE, Lord K, Lipman TH (2012) The epidemiology of type 1 diabetes in children. Endocrinol Metab Clin N Am 41:679–694
44. Viskari HR, Koskela P, Lonnrot M et al (2000) Can enterovirus infections explain the increasing incidence of type 1 diabetes? Diabetes Care 23:414–416
45. Achenbach P, Bonifacio E, Koczwara K, Ziegler AG (2005) Natural history of type 1 diabetes. Diabetes 54(Suppl 2):S25–S31
46. Cakir M, Akcay S, Karakas T, Gedik Y, Okten A, Orhan F (2008) Prevalence of atopy in children with type 1 diabetes mellitus, hepatitis B virus carriers, and healthy children: role of T helper 1 (Th1)-type immune response. Allergy Asthma Proc 29:166–170
47. Tzeng ST, Hsu SG, Fu LS, Chi CS (2007) Prevalence of atopy in children with type 1 diabetes mellitus in central Taiwan. J Microbiol Immunol Infect 40:74–78
48. Craighead JE, McLane MF (1968) Diabetes mellitus: induction in mice by encephalomyocarditis virus. Science 162:913–914
49. Ylipaasto P, Smura T, Gopalacharyulu P et al (2012) Enterovirus-induced gene expression profile is critical for human pancreatic islet destruction. Diabetologia 55:3273–3283