Skip to main content

Advertisement

SpringerLink
Log in
Menu
Find a journal Publish with us Track your research
Search
Cart
  1. Home
  2. Photochemical & Photobiological Sciences
  3. Article

Are low sun exposure and/or vitamin D risk factors for type 1 diabetes?

  • Perspective
  • Open access
  • Published: 27 October 2020
  • Volume 16, pages 381–398, (2017)
  • Cite this article
Download PDF

You have full access to this open access article

Photochemical & Photobiological Sciences Aims and scope Submit manuscript
Are low sun exposure and/or vitamin D risk factors for type 1 diabetes?
Download PDF
  • K. M. Miller1,
  • P. H. Hart1,
  • N. H. de Klerk1,
  • E. A. Davis2 &
  • …
  • R. M. Lucas3 
  • 161 Accesses

  • 16 Citations

  • 22 Altmetric

  • 2 Mentions

  • Explore all metrics

Abstract

The global variation in type 1 diabetes (T1D) incidence rates is one of the most significant observed for any non-communicable disease. Geographical patterns in incidence suggest that low sun exposure may contribute to the wide disparity, with incidence rates generally increasing with distance from the Equator. T1D development is associated with hyperactivity of the adaptive immune system leading to autoimmune destruction of insulin-secreting pancreatic β cells. Both exposure to ultraviolet radiation (UVR) and vitamin D, with their known immunosuppressive effects, have the potential to delay or inhibit the disease. Efforts to confirm the role of UVR by vitamin D dependent and independent pathways in the pathogenesis of T1D have been challenged by inconsistent results among studies. Human observational studies and animal and in vitro experiments indicate that at least some of the benefits of sun exposure come from improved vitamin D status. There is no evidence of benefit for T1D risk of vitamin D supplementation during pregnancy at current recommended levels (400 IU per day); but some evidence supports that higher sun exposure and/or vitamin D sufficiency in pregnancy, or supplementation in early life, decreases T1D risk. Further research is required to confirm an association between UVR exposure and T1D and clarify the mechanisms involved.

Article PDF

Download to read the full article text

Similar content being viewed by others

Evidence-based European recommendations for the dietary management of diabetes

Article 17 April 2023

The Diabetes and Nutrition Study Group (DNSG) of the European Association for the Study of Diabetes (EASD)

Global trends in diabetes complications: a review of current evidence

Article 31 August 2018

Jessica L. Harding, Meda E. Pavkov, … Edward W. Gregg

Environment, Lifestyle, and Female Infertility

Article 03 August 2020

Renu Bala, Vertika Singh, … Kiran Singh

Use our pre-submission checklist

Avoid common mistakes on your manuscript.

References

  1. H. J. Aanstoot, B. J. Anderson, D. Daneman, T. Danne, K. Donaghue, F. Kaufman, R. R. Rea, and Y. Uchigata Pediatr. Diabetes, 2007, 8, Suppl 8 1–44

    PubMed  Google Scholar 

  2. International Diabetes Federation, International Diabetes Federation Atlas, Brussels, 2015

    Google Scholar 

  3. E. A. Spaans, L. Gusdorf, K. H. Groenier, P. L. Brand, H. J. Veeze, H. M. Reeser, H. J. Bilo, and N. Kleefstra Acta Paediatr., 2015, 104, 626–629

    Article  PubMed  Google Scholar 

  4. T. H. Lipman, L. E. L. Katz, S. J. Ratcliffe, K. M. Murphy, A. Aguilar, I. Rezvani, C. J. Howe, S. Fadia, and E. Suarez Diabetes Care, 2013, 36, 1597–1603

    Article  PubMed  PubMed Central  Google Scholar 

  5. G. Bruno, M. Maule, A. Biggeri, A. Ledda, C. Mannu, F. Merletti, and M. Songini Diabetes, 2013, DB_121771

    Google Scholar 

  6. S. B. Mohr, C. F. Garland, E. D. Gorham and F. C. Garland Diabetologia, 2008, 51, 1391–1398

    Article  CAS  PubMed  Google Scholar 

  7. M. T. Cantorna Proc. Soc. Exp. Biol. Med., 2000, 223, 230–233

    Article  CAS  PubMed  Google Scholar 

  8. M. F. Holick J. Clin. Invest., 2006, 116, 2062–2072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Institute of Medicine, Dietary reference intakes for calcium and vitamin D, The National Academies Press, Washington, DC, 2011

    Google Scholar 

  10. I. M. Sørensen, G. Joner, P. A. Jenum, A. Eskild, C. Brunborg, P. A. Torjesen and L. C. Stene Diabetes/Metab. Res. Rev., 2016, 32, 883–890

    Article  CAS  Google Scholar 

  11. I. M. Sorensen, G. Joner, P. A. Jenum, A. Eskild, P. A. Torjesen and L. C. Stene Diabetes, 2012, 61, 175–178

    Article  PubMed  CAS  Google Scholar 

  12. J. Y. Dong, W. G. Zhang, J. J. Chen, Z. L. Zhang, S. F. Han and L. Q. Qin Nutrients, 2013, 5, 3551–3562

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. H. Glerup, K. Mikkelsen, L. Poulsen, E. Hass, S. Overbeck, J. Thomsen, P. Charles and E. F. Eriksen J. Intern. Med., 2000, 247, 260–268

    Article  CAS  PubMed  Google Scholar 

  14. M. F. Holick and T. C. Chen Am. J. Clin. Nutr., 2008, 87, 1080S–1086S

    Article  CAS  PubMed  Google Scholar 

  15. M. L. Kripke Cancer Res., 1994, 54, 6102–6105

    CAS  PubMed  Google Scholar 

  16. EURODIAB ACE Study Group Diabetologia, 1999, 42, 51–54

    Article  Google Scholar 

  17. C. S. Zipitis and A. K. Akobeng Arch. Dis. Child., 2008, 93, 512–517

    Article  CAS  PubMed  Google Scholar 

  18. T. L. van Belle, K. T. Coppieters, M. G. von Herrath Physiol. Rev., 2011, 91, 79–118

    Article  PubMed  CAS  Google Scholar 

  19. M. E. Craig, C. Jefferies, D. Dabelea, N. Balde, A. Seth and K. C. Donaghue Pediatr. Diabetes, 2014, 15, 4–17

    Article  CAS  PubMed  Google Scholar 

  20. J. J. Couper, M. J. Haller, A. G. Ziegler, M. Knip, J. Ludvigsson and M. E. Craig Pediatr. Diabetes, 2014, 15, 18–25

    Article  CAS  PubMed  Google Scholar 

  21. Baker IDI Heart and Diabetes Institute, Diabetes: the silent pandemic and its impact on Australia, Novo Nordisk Pharmaceuticals Pty Ltd, New South Wales, 2012

    Google Scholar 

  22. Australian Institute of Health and Welfare, Incidence of type 1 diabetes in Australia 2000–2013, Report Diabetes series no. 23, AIHW, Canberra, 2015

    Google Scholar 

  23. J. Fairchild J. Paediatr. Child Health, 2015, 51, 122–125

    Article  PubMed  Google Scholar 

  24. A. Butwicka, L. Frisén, C. Almqvist, B. Zethelius, and P. Lichtenstein Diabetes Care, 2015, 38, 453–459

    Article  PubMed  PubMed Central  Google Scholar 

  25. C. Patterson, G. Dahlquist, V. Harjutsalo, G. Joner, R. Feltbower, J. Svensson, E. Schober, E. Gyürüs, C. Castell and B. Urbonaité Diabetologia, 2007, 50, 2439–2442

    Article  CAS  PubMed  Google Scholar 

  26. G. Dahlquist, and B. Kallen Diabetes Care, 2005, 28, 2384–2387

    Article  PubMed  Google Scholar 

  27. T. Skrivarhaug, H.-J. Bangstad, L. Stene, L. Sandvik, K. Hanssen, and G. Joner Diabetologia, 2006, 49, 298–305

    Article  CAS  PubMed  Google Scholar 

  28. V. Harjutsalo, C. Forsblom and P.-H. Groop Br. Med. J. (Clin. Res. Ed.), 2011, 343, d5364

    Article  Google Scholar 

  29. S. J. Livingstone, D. Levin, H. C. Looker, R. S. Lindsay, S. H. Wild, N. Joss, G. Leese, P. Leslie, R. J. McCrimmon, and W. Metcalfe J. Am. Med. Assoc., 2015, 313, 37–44

    Article  CAS  Google Scholar 

  30. M. Katz, and L. Laffel J. Am. Med. Assoc., 2015, 313, 35–36

    Article  CAS  Google Scholar 

  31. J. C. Elliott, R. M. Lucas, M. S. Clements and H. J. Bambrick Pediatr. Diabetes, 2010, 11, 394–402

    Article  PubMed  Google Scholar 

  32. M. Rewers, and J. Ludvigsson Lancet, 2016, 387, 2340–2348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. P. Concannon, S. S. Rich and G. T. Nepom N. Engl. J. Med., 2009, 360, 1646–1654

    Article  CAS  PubMed  Google Scholar 

  34. F. Pociot, Å. Lernmark Lancet, 2016, 387, 2331–2339

    Article  CAS  PubMed  Google Scholar 

  35. M. Knip, R. Veijola, S. M. Virtanen, H. Hyöty, O. Vaarala and H. K. Åkerblom Diabetes, 2005, 54, S125–S136

    Article  CAS  PubMed  Google Scholar 

  36. A. Barnett, C. Eff, R. D. Leslie, and D. Pyke Diabetologia, 1981, 20, 87–93

    Article  CAS  PubMed  Google Scholar 

  37. M. Redondo, L. Yu, M. Hawa, T. Mackenzie, D. Pyke, G. Eisenbarth, and R. Leslie Diabetologia, 2001, 44, 354–362

    Article  CAS  PubMed  Google Scholar 

  38. J. Kaprio, J. Tuomilehto, M. Koskenvuo, K. Romanov, A. Reunanen, J. Eriksson, J. Stengård and Y. Kesäniemi Diabetologia, 1992, 35, 1060–1067

    Article  CAS  PubMed  Google Scholar 

  39. V. Hyttinen, J. Kaprio, L. Kinnunen, M. Koskenvuo, and J. Tuomilehto Diabetes, 2003, 52, 1052–1055

    Article  CAS  PubMed  Google Scholar 

  40. P. Olmos, R. A’hern, D. Heaton, B. Millward, D. Risley, D. Pyke, and R. Leslie Diabetologia, 1988, 31, 747–750

    Article  CAS  PubMed  Google Scholar 

  41. E. Hypponen Diabetes, Obes. Metab., 2010, 12, 737–743

    Article  CAS  Google Scholar 

  42. Diamond Project Group Diabetic Med., 2006, 23, 857

    Article  Google Scholar 

  43. M. A. Atkinson, G. S. Eisenbarth and A. W. Michels Lancet, 2014, 383, 69–82

    Article  PubMed  Google Scholar 

  44. J. Ahn, K. Yu, R. Stolzenberg-Solomon, K. C. Simon, M. L. McCullough, L. Gallicchio, E. J. Jacobs, A. Ascherio, K. Helzlsouer and K. B. Jacobs Hum. Mol. Genet., 2010, ddq155

    Google Scholar 

  45. A. Leandro, M. Rocha, C. Cardoso and M. Bonecini-Almeida Braz. J. Med. Biol. Res., 2009, 42, 312–322

    Article  CAS  PubMed  Google Scholar 

  46. P. Selvaraj Vitam. Horm., 2010, 86, 307–325

    Article  CAS  Google Scholar 

  47. A. G. Uitterlinden, Y. Fang, J. B. van Meurs, H. A. Pols and J. P. van Leeuwen Gene, 2004, 338, 143–156

    Article  CAS  PubMed  Google Scholar 

  48. J. M. Valdivielso, and E. Fernandez Clin. Chim. Acta, 2006, 371, 1–12

    Article  CAS  PubMed  Google Scholar 

  49. P. Chocano-Bedoya and A. G. Ronnenberg Nutr. Rev., 2009, 67, 289–293

    Article  PubMed  Google Scholar 

  50. L. C. Stene, J. Ulriksen, P. Magnus, and G. Joner Diabetologia, 2000, 43, 1093–1098

    Article  CAS  PubMed  Google Scholar 

  51. L. C. Stene, and G. Joner Am. J. Clin. Nutr., 2003, 78, 1128–1134

    Article  CAS  PubMed  Google Scholar 

  52. L. Marjamaki, S. Niinisto, M. G. Kenward, L. Uusitalo, U. Uusitalo, M. L. Ovaskainen, C. Kronberg-Kippila, O. Simell, R. Veijola, J. Ilonen, M. Knip and S. M. Virtanen Diabetologia, 2010, 53, 1599–1607

    Article  CAS  PubMed  Google Scholar 

  53. M. Granfors, H. Augustin, J. Ludvigsson and H. K. Brekke Pediatr. Diabetes, 2015, 17, 525–530

    Article  PubMed  CAS  Google Scholar 

  54. H. K. Brekke, and J. Ludvigsson Pediatr. Diabetes, 2007, 8, 11–14

    Article  PubMed  Google Scholar 

  55. C. M. Fronczak, A. E. Baron, H. P. Chase, C. Ross, H. L. Brady, M. Hoffman, G. S. Eisenbarth, M. Rewers and J. M. Norris Diabetes Care, 2003, 26, 3237–3242

    Article  PubMed  Google Scholar 

  56. B. A. Wicklow and S. P. Taback Ann. N. Y. Acad. Sci., 2006, 1079, 310–312

    Article  CAS  PubMed  Google Scholar 

  57. M. T. Tenconi, G. Devoti, M. Comelli, M. Pinon, A. Capocchiano, V. Calcaterra, and G. Pretti Acta Diabetol., 2007, 44, 14–19

    Article  CAS  PubMed  Google Scholar 

  58. N. Visalli, L. Sebastiani, E. Adorisio, A. Conte, A. De Cicco, R. D’Elia, S. Manfrini, P. Pozzilli, and I. Group Arch. Dis. Child., 2003, 88, 695–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. E. Hypponen, E. Laara, A. Reunanen, M. R. Jarvelin and S. M. Virtanen Lancet, 2001, 358, 1500–1503

    Article  CAS  PubMed  Google Scholar 

  60. A. L. Ponsonby, R. M. Lucas and I. A. van der Mei Photochem. Photobiol., 2005, 81, 1267–1275

    Article  CAS  PubMed  Google Scholar 

  61. S. S. Harris Am. J. Clin. Nutr., 2004, 79, 889–890

    Article  CAS  PubMed  Google Scholar 

  62. G. K. Schwalfenberg J. Environ. Public Health, 2012, 2012, 619381

    PubMed  PubMed Central  Google Scholar 

  63. H. Vatanparast, J. L. Adolphe and S. J. Whiting Health Rep., 2010, 21, 19

    PubMed  Google Scholar 

  64. J. D. Cooper, D. J. Smyth, N. M. Walker, H. Stevens, O. S. Burren, C. Wallace, C. Greissl, E. Ramos-Lopez, E. Hyppönen and D. B. Dunger Diabetes, 2011, 60, 1624–1631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. B. N. Frederiksen, M. Kroehl, T. E. Fingerlin, R. Wong, A. K. Steck, M. Rewers and J. M. Norris J. Clin. Endocrinol. Metab., 2013, 98, E1845–E1851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. E. R. Lopez, O. Zwermann, M. Segni, G. Meyer, M. Reincke, J. Seissler, J. Herwig, K.-H. Usadel, and K. Badenhoop Eur. J. Endocrinol., 2004, 151, 193–197

    Article  CAS  PubMed  Google Scholar 

  67. S. H. Abd-Allah, H. F. Pasha, H. A. Hagrass and A. A. Alghobashy Gene, 2014, 536, 430–434

    Article  CAS  PubMed  Google Scholar 

  68. M. E. Miettinen, M. C. Smart, L. Kinnunen, C. Mathews, V. Harjutsalo, H. M. Surcel, C. Lamberg-Allardt, J. Tuomilehto and G. A. Hitman Diabetologia, 2015, 58, 2278–2283

    Article  CAS  PubMed  Google Scholar 

  69. K. Tizaoui, W. Kaabachi, A. Hamzaoui, and K. Hamzaoui J. Steroid Biochem. Mol. Biol., 2014, 143, 240–249

    Article  CAS  PubMed  Google Scholar 

  70. E. Ramos-Lopez, P. Brück, T. Jansen, J. M. Pfeilschifter, H. H. Radeke, and K. Badenhoop J. Steroid Biochem. Mol. Biol., 2007, 103, 807–810

    Article  CAS  PubMed  Google Scholar 

  71. L. Reinert-Hartwall, J. Honkanen, T. Härkönen, J. Ilonen, O. Simell, A. Peet, V. Tillmann, C. Lamberg-Allardt, S. Virtanen, and M. Knip Diabetes/Metab. Res. Rev., 2014, 30, 749–760

    Article  CAS  Google Scholar 

  72. S. Mauf, M. Penna-Martinez, T. Jentzsch, H. Ackermann, D. Henrich, H. H. Radeke, P. Brück, K. Badenhoop and E. Ramos-Lopez J. Steroid Biochem. Mol. Biol., 2015, 147, 17–23

    Article  CAS  PubMed  Google Scholar 

  73. A.-L. Ponsonby, A. Pezic, J. Ellis, R. Morley, F. Cameron, J. Carlin, and T. Dwyer Am. J. Epidemiol., 2008, 168, 358–365

    Article  PubMed  Google Scholar 

  74. R. J. Wilkinson, M. Llewelyn, Z. Toossi, P. Patel, G. Pasvol, A. Lalvani, D. Wright, M. Latif and R. N. Davidson Lancet, 2000, 355, 618–621

    Article  CAS  PubMed  Google Scholar 

  75. J. B. Zella, L. C. McCary and H. F. DeLuca Arch. Biochem. Biophys., 2003, 417, 77–80

    Article  CAS  PubMed  Google Scholar 

  76. A. Giulietti, C. Gysemans, K. Stoffels, E. van Etten, B. Decallonne, L. Overbergh, R. Bouillon, and C. Mathieu Diabetologia, 2004, 47, 451–462

    Article  CAS  PubMed  Google Scholar 

  77. C. Mathieu, J. Laureys, H. Sobis, M. Vandeputte, M. Waer, and R. Bouillon Diabetes, 1992, 41, 1491–1495

    Article  CAS  PubMed  Google Scholar 

  78. C. Mathieu, M. Waer, J. Laureys, O. Rutgeerts, and R. Bouillon Diabetologia, 1994, 37, 552–558

    Article  CAS  PubMed  Google Scholar 

  79. C. Mathieu, M. Waer, K. Casteels, J. Laureys, and R. Bouillon Endocrinology, 1995, 136, 866–872

    Article  CAS  PubMed  Google Scholar 

  80. J. P. Driver, O. Foreman, C. Mathieu, E. Van Etten and D. V. Serreze Clin. Exp. Immunol., 2008, 151, 76–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. M. T. Cantorna Arch. Biochem. Biophys., 2012, 523, 103–106

    Article  CAS  PubMed  Google Scholar 

  82. M. Hawa, M. Valorani, L. Buckley, P. Beales, A. Afeltra, F. Cacciapaglia, R. Leslie, and P. Pozzilli Horm. Metab. Res., 2004, 36, 620–624

    Article  CAS  PubMed  Google Scholar 

  83. T. Takiishi, L. Ding, F. Baeke, I. Spagnuolo, G. Sebastiani, J. Laureys, A. Verstuyf, G. Carmeliet, F. Dotta, T. L. Van Belle, C. A. Gysemans, and C. Mathieu Diabetes, 2014, 63, 2026–2036

    Article  CAS  PubMed  Google Scholar 

  84. C. Mathieu, E. van Etten, C. Gysemans, B. Decallonne, and R. Bouillon Lancet, 2002, 359, 1248

    Article  PubMed  Google Scholar 

  85. C. A. Gysemans, A. K. Cardozo, H. Callewaert, A. Giulietti, L. Hulshagen, R. Bouillon, D. L. Eizirik, and C. Mathieu Endocrinology, 2005, 146, 1956–1964

    Article  CAS  PubMed  Google Scholar 

  86. K. M. Casteels, C. Mathieu, M. Waer, D. Valckx, L. Overbergh, J. M. Laureys, and R. Bouillon Endocrinology, 1998, 139, 95–102

    Article  CAS  PubMed  Google Scholar 

  87. S. Gregori, N. Giarratana, S. Smiroldo, M. Uskokovic, and L. Adorini Diabetes, 2002, 51, 1367–1374

    Article  CAS  PubMed  Google Scholar 

  88. N. Giarratana, G. Penna, S. Amuchastegui, R. Mariani, K. C. Daniel, and L. Adorini J. Immunol., 2004, 173, 2280–2287

    Article  CAS  PubMed  Google Scholar 

  89. K. Casteels, M. Waer, J. Laureys, D. Valckx, J. Depovere, R. Bouillon, and C. Mathieu Transplantation, 1998, 65, 1225–1232

    Article  CAS  PubMed  Google Scholar 

  90. L. E. Schneider, H. P. Schedl, T. McCain and M. R. Haussler Science, 1977, 196, 1452–1454

    Article  CAS  PubMed  Google Scholar 

  91. B. L. Nyomba, R. Bouillon, W. Lissens, H. V. Baellen and P. D. Moor Endocrinology, 1985, 116, 2483–2488

    Article  CAS  PubMed  Google Scholar 

  92. K. Ikeda, T. Matsumoto, K. Morita, H. Yamato, H. Takahashi, I. Ezawa, and E. Ogata Endocrinology, 1987, 121, 1721–1726

    Article  CAS  PubMed  Google Scholar 

  93. K. Ikeda, T. Matsumoto, K. Morita, Y. Kawanobe, I. Ezawa, and E. Ogata Metabolism, 1987, 36, 555–557

    Article  CAS  PubMed  Google Scholar 

  94. S. Hough, A. Fauso, Y. Sonn, O. Dong Jo, S. J. Birge and L. V. Avioli Endocrinology, 1983, 113, 790–796

    Article  CAS  PubMed  Google Scholar 

  95. E. M. Spencer, M. Khalil, and O. Tobiassen Endocrinology, 1980, 107, 300–305

    Article  CAS  PubMed  Google Scholar 

  96. H. Ishida, Y. Seino, K. Tsuda, J. Takemura, S. Nishi, S. Ishizuka, and H. Imura Acta Endocrinol., 1983, 104, 96–102

    Article  CAS  Google Scholar 

  97. R. Bland, D. Markovic, C. E. Hills, S. V. Hughes, S. L. Chan, P. E. Squires, and M. Hewison J. Steroid Biochem. Mol. Biol., 2004, 89, 121–125

    Article  PubMed  CAS  Google Scholar 

  98. B. Maestro, N. Dávila, M. C. Carranza, and C. Calle J. Steroid Biochem. Mol. Biol., 2003, 84, 223–230

    Article  CAS  PubMed  Google Scholar 

  99. C. Becker, J. Kubach, J. Wijdenes, J. Knop, and H. Jonuleit Eur. J. Immunol., 2007, 37, 1217–1223

    Article  CAS  PubMed  Google Scholar 

  100. Y. Morán-Auth, M. Penna-Martinez, and K. Badenhoop J. Steroid Biochem. Mol. Biol., 2015, 148, 184–186

    Article  PubMed  CAS  Google Scholar 

  101. D. d. Mauricio, H. U. Andersen, C. M. Larsen, A. E. Karlsen, T. Mandrup-Poulsen, and J. Nerup Cytokine, 1997, 9, 563–569

    Article  CAS  PubMed  Google Scholar 

  102. S. Sandler, K. Buschard, and K. Bendtzen Immunol. Lett., 1994, 41, 73–77

    Article  CAS  PubMed  Google Scholar 

  103. R. Riachy, B. Vandewalle, S. Belaich, J. Kerr-Conte, V. Gmyr, F. Zerimech, M. d’Herbomez, J. Lefebvre, and F. Pattou J. Endocrinol., 2001, 169, 161–168

    Article  CAS  PubMed  Google Scholar 

  104. R. Riachy, B. Vandewalle, J. Kerr Conte, E. Moerman, P. Sacchetti, B. Lukowiak, V. Gmyr, T. Bouckenooghe, M. Dubois, and F. Pattou Endocrinology, 2002, 143, 4809–4819

    Article  CAS  PubMed  Google Scholar 

  105. R. Riachy, B. Vandewalle, E. Moerman, S. Belaich, B. Lukowiak, V. Gmyr, G. Muharram, J. K. Conte, and F. Pattou Apoptosis, 2006, 11, 151–159

    Article  CAS  PubMed  Google Scholar 

  106. M. Chakhtoura and S. T. Azar Int. J. Endocrinol., 2013, 2013, 148673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. G. Dahlquist, and L. Mustonen Int. J. Epidemiol., 1994, 23, 1234–1241

    Article  CAS  PubMed  Google Scholar 

  108. L. J. Black, S. A. Burrows, P. Jacoby, W. H. Oddy, L. J. Beilin, W. Chan She Ping-Delfos, C. E. Marshall, P. G. Holt, P. H. Hart and T. A. Mori Br. J. Nutr., 2014, 112, 1154–1162

    Article  CAS  PubMed  Google Scholar 

  109. G. Jones, C. Blizzard, M. D. Riley, V. Parameswaran, T. M. Greenaway, and T. Dwyer Eur. J. Clin. Nutr., 1999, 53, 824–829

    Article  CAS  PubMed  Google Scholar 

  110. J. A. Staples, A. L. Ponsonby, L. L. Lim and A. J. McMichael Environ. Health Perspect., 2003, 111, 518–523

    Article  PubMed  PubMed Central  Google Scholar 

  111. S. J. Ball, A. Haynes, P. Jacoby, G. Pereira, L. J. Miller, C. Bower and E. A. Davis Health Place, 2014, 28, 194–204

    Article  PubMed  Google Scholar 

  112. L. Nyström, G. Dahlquist, J. Östman, S. Wall, H. Arnqvist, G. Blohme, F. Lithner, B. Littorin, B. Schersten, and L. Wibell Int. J. Epidemiol., 1992, 21, 352–358

    Article  PubMed  Google Scholar 

  113. G. Joner, L. C. Stene, O. Søvik Diabetes Care, 2004, 27, 1618–1622

    Article  PubMed  Google Scholar 

  114. Z. Yang, K. Wang, T. Li, W. Sun, Y. Li, Y.-F. Chang, J. S. Dorman and R. E. LaPorte Diabetes Care, 1998, 21, 525–529

    Article  CAS  PubMed  Google Scholar 

  115. C. Patterson, G. Dahlquist, G. Soltesz, A. Green, E. A. S. Group Diabetologia, 2001, 44, B9–B16

    Article  PubMed  Google Scholar 

  116. J. Tuomilehto, T. Podar, A. Reunanen, I. Kalits, R. Lounamaa, E. Tuomilehto-Wolf, B. Adojaan, B. Neff and R. E. LaPorte Diabetes Care, 1991, 14, 982–988

    Article  CAS  PubMed  Google Scholar 

  117. M. Karvonen, M. Viik-Kajander, E. Moltchanova, I. Libman, R. LaPorte, and J. Tuomilehto Diabetes Care, 2000, 23, 1516–1526

    Article  CAS  PubMed  Google Scholar 

  118. U. Söderström, J. Åman, and A. Hjern Acta Paediatr., 2012, 101, 73–77

    Article  PubMed  Google Scholar 

  119. A. T. Borchers, R. Uibo, and M. Gershwin Autoimmun. Rev., 2010, 9, A355–A365

    Article  PubMed  Google Scholar 

  120. M. Songini, A. Casu, I. Ashkenazi, and Z. Laron J. Pediatr. Endocrinol. Metab., 2001, 14, 781–784

    Article  CAS  PubMed  Google Scholar 

  121. H. S. Kahn, T. M. Morgan, L. D. Case, D. Dabelea, E. J. Mayer-Davis, J. M. Lawrence, S. M. Marcovina, G. Imperatore and S. f. D. i. Y. S. Group Diabetes Care, 2009, 32, 2010–2015

    Article  PubMed  PubMed Central  Google Scholar 

  122. M. I. Kalliora, A. Vazeou, D. Delis, E. Bozas, I. Thymelli and C. S. Bartsocas Hormones, 2011, 10, 67–71

    Article  PubMed  Google Scholar 

  123. P. Rothwell, A. Staines, P. Smail, E. Wadsworth, and P. McKinney Br. Med. J., 1996, 312, 1456

    Article  CAS  Google Scholar 

  124. P. M. Rothwell, S. A. Gutnikov, P. A. McKinney, E. Schober, C. Ionescu-Tirgoviste, and A. Neu Br. Med. J. (Clin. Res. Ed.), 1999, 319, 887–888

    Article  CAS  Google Scholar 

  125. U. Samuelsson, C. Johansson, and J. Ludvigsson Arch. Dis. Child., 1999, 81, 143–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. A. G. Schranz Diabetes Care, 1998, 21, 194–195

    Article  CAS  PubMed  Google Scholar 

  127. A. M. Vaiserman, B. Carstensen, V. P. Voitenko, M. D. Tronko, V. I. Kravchenko, M. D. Khalangot and L. V. Mechova Diabetologia, 2007, 50, 32–35

    Article  CAS  PubMed  Google Scholar 

  128. O. Kordonouri, N. Shuga, H. Lewy, I. Ashkenazi, and Z. Laron Eur. J. Pediatr., 2002, 161, 291–292

    Article  PubMed  Google Scholar 

  129. J. Ye, R.-G. Chen, I. Ashkenazi, and Z. Laron J. Pediatr. Endocrinol. Metab., 1998, 11, 461–464

    Article  CAS  PubMed  Google Scholar 

  130. G. Dahlquist, L. Blom, G. Holmgren, B. Hagglof, Y. Larsson, G. Sterky, and S. Wall Diabetologia, 1985, 28, 802–808

    Article  CAS  PubMed  Google Scholar 

  131. P. H. Jongbloet, H. M. Groenewoud, R. A. Hirasing and S. Van Buuren Diabetes Care, 1998, 21, 190–191

    Article  CAS  PubMed  Google Scholar 

  132. Z. Laron, H. Lewy, I. Wilderman, A. Casu, J. Willis, M. J. Redondo, I. Libman, N. White, and M. Craig Isr. Med. Assoc. J., 2005, 7, 381–384

    PubMed  Google Scholar 

  133. E. F. Roche, H. Lewy, H. M. Hoey, and Z. Laron J. Pediatr. Endocrinol. Metab., 2003, 16, 779–782

    Article  PubMed  Google Scholar 

  134. G. G. Dahlquist and B. A. Kallen Diabetes Care, 1996, 19, 328–332

    Article  CAS  PubMed  Google Scholar 

  135. T. Bock, C. R. Pedersen, A. Volund, C. S. Pallesen, and K. Buschard Diabetes Care, 1994, 17, 1154–1157

    Article  CAS  PubMed  Google Scholar 

  136. P. A. McKinney Diabetologia, 2001, 44, Suppl 3 B67–B74

    Article  PubMed  Google Scholar 

  137. K. Kida, G. Mimura, T. Ito, K. Murakami, I. Ashkenazi, and Z. Laron Diabetic Med., 2000, 17, 59–63

    Article  CAS  PubMed  Google Scholar 

  138. W. B. Grant and M. F. Holick Altern. Med. Rev., 2005, 10, 94–111

    PubMed  Google Scholar 

  139. S. Whiting, K. Langlois, and H. Vatanparast Am. J. Clin. Nutr., 2011, 94, 128–135

    Article  CAS  PubMed  Google Scholar 

  140. F. Cadario, S. Savastio, V. Pagliardini, M. Bagnati, M. Vidali, F. Cerutti, I. Rabbone, F. Fontana, R. Lera, V. De Donno, A. Valori, G. Gruden, G. Bona, and G. Bruno Acta Diabetol., 2015, 52, 1077–1081

    Article  CAS  PubMed  Google Scholar 

  141. E. V. Moltchanova, N. Schreier, N. Lammi, and M. Karvonen Diabetic Med., 2009, 26, 673–678

    Article  CAS  PubMed  Google Scholar 

  142. A. Neu, M. Kehrer, R. Hub and M. B. Ranke Diabetes Care, 1997, 20, 530–533

    Article  CAS  PubMed  Google Scholar 

  143. J. Mooney, P. Helms, I. Jolliffe, and P. Smail Arch. Dis. Child., 2004, 89, 970–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. T. Waldhoer, E. Schober, and J. Tuomilehto J. Clin. Epidemiol., 1997, 50, 159–165

    Article  CAS  PubMed  Google Scholar 

  145. C. Patterson, E. Gyurus, J. Rosenbauer, O. Cinek, A. Neu, E. Schober, R. Parslow, G. Joner, J. Svensson, C. Castell, P. Bingley, E. Schoenle, P. Jarosz-Chobot, B. Urbonaite, U. Rothe, C. Krzisnik, C. Ionescu-Tirgoviste, I. Weets, M. Kocova, G. Stipancic, M. Samardzic, C. de Beaufort, A. Green, G. Soltesz, and G. Dahlquist Pediatr. Diabetes, 2014, 16, 573–580

    Article  PubMed  Google Scholar 

  146. C. Glatthaar, D. E. Whittall, T. A. Welborn, M. J. Gibson, B. H. Brooks, M. M. Ryan and G. C. Byrne Med. J. Aust., 1988, 148, 117–123

    Article  CAS  PubMed  Google Scholar 

  147. J. Santos, E. Carrasco, A. Moore, F. Perez-Bravo, and C. Albala Rev. Saude Publica, 2001, 35, 96–100

    Article  CAS  PubMed  Google Scholar 

  148. R. S. Scott, L. J. Brown, B. A. Darlow, L. V. Forbes and M. P. Moore Diabetes Care, 1992, 15, 895–899

    Article  CAS  PubMed  Google Scholar 

  149. G. Soltesz, C. Patterson, and G. Dahlquist Pediatr. Diabetes, 2007, 8, 6–14

    Article  PubMed  Google Scholar 

  150. J. A. Willis, R. S. Scott, B. A. Darlow, H. Lewy, I. Ashkenazi, and Z. Laron J. Pediatr. Endocrinol. Metab., 2002, 15, 645–647

    PubMed  Google Scholar 

  151. P. Durruty, F. Ruiz, M. Garcia de los Rios Diabetologia, 1979, 17, 357–360

    Article  CAS  PubMed  Google Scholar 

  152. U. Samuelsson, J. Carstensen, O. Lofman, and S. Nordfeldt Diabetes Res. Clin. Pract., 2007, 76, 75–81

    Article  CAS  PubMed  Google Scholar 

  153. S. Sloka, M. Grant and L. A. Newhook Acta Diabetol., 2010, 47, 73–78

    Article  PubMed  Google Scholar 

  154. C. Levy-Marchal, C. Patterson, and A. Green Diabetologia, 1995, 38, 823–830

    Article  CAS  PubMed  Google Scholar 

  155. M. Karvonen, V. Jäntti, S. Muntoni, M. Stabilini, L. Stabilini, S. Muntoni, and J. Tuomilehto Diabetes Care, 1998, 21, 1101–1109

    Article  CAS  PubMed  Google Scholar 

  156. E. Schober, and H. Frisch Acta Paediatr., 1988, 77, 299–302

    Article  CAS  Google Scholar 

  157. I. Waernbaum, and G. Dahlquist Eur. J. Epidemiol., 2015, 1–5

    Google Scholar 

  158. T. Takiishi, C. Gysemans, R. Bouillon, and C. Mathieu Rheum. Dis. Clin. North Am., 2012, 38, 179–206

    Article  PubMed  Google Scholar 

  159. R. Jacobsen, S. U. Thorsen, A. S. Cohen, M. Lundqvist, P. Frederiksen, C. B. Pipper, F. Pociot, L. C. Thygesen, A. Ascherio, and J. Svensson Diabetologia, 2016, 1–11

    Google Scholar 

  160. M. E. Miettinen, L. Reinert, L. Kinnunen, V. Harjutsalo, P. Koskela, H. M. Surcel, C. Lamberg-Allardt, and J. Tuomilehto Diabetologia, 2012, 55, 1291–1294

    Article  CAS  PubMed  Google Scholar 

  161. Commonwealth of Australia and New Zealand Government, Nutrient Reference Values for Australia and New Zealand, Canberra, 2005

    Google Scholar 

  162. B. R. Becklund, K. S. Severson, S. V. Vang and H. F. DeLuca Proc. Natl. Acad. Sci. U.S.A., 2010, 107, 6418–6423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. R. M. Lucas, A. L. Ponsonby, K. Dear, P. C. Valery, M. P. Pender, B. V. Taylor, T. J. Kilpatrick, T. Dwyer, A. Coulthard, C. Chapman, I. van der Mei, D. Williams and A. J. McMichael Neurology, 2011, 76, 540–548

    Article  CAS  PubMed  Google Scholar 

  164. P. H. Hart, S. Gorman, J. J. Finlay-Jones Nat. Rev. Immunol., 2011, 11, 584–596

    Article  CAS  PubMed  Google Scholar 

  165. S. E. Ullrich and S. N. Byrne J. Invest. Dermatol., 2012, 132, 896–905

    Article  CAS  PubMed  Google Scholar 

  166. R. L. Ng, J. L. Bisley, S. Gorman, M. Norval and P. H. Hart J. Immunol., 2010, 185, 7207–7215

    Article  CAS  PubMed  Google Scholar 

  167. R. L. Ng, N. M. Scott, D. H. Strickland, S. Gorman, M. A. Grimbaldeston, M. Norval, J. Waithman and P. H. Hart J. Immunol., 2013, 190, 5471–5484

    Article  CAS  PubMed  Google Scholar 

  168. P. H. Hart, M. A. Grimbaldeston, G. J. Swift, A. Jaksic, F. P. Noonan, J. J. Finlay-Jones J. Exp. Med., 1998, 187, 2045–2053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. R. Chacón-Salinas, A. Y. Limón-Flores, A. D. Chávez-Blanco, A. Gonzalez-Estrada and S. E. Ullrich J. Immunol., 2011, 186, 25–31

    Article  PubMed  CAS  Google Scholar 

  170. T. Takiishi, T. Van Belle, C. Gysemans, and C. Mathieu Pediatr. Diabetes, 2013, 14, 81–89

    Article  CAS  PubMed  Google Scholar 

  171. S. Gorman, M. A. Judge, J. T. Burchell, D. J. Turner and P. H. Hart Immunology, 2010, 130, 181–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. L. Biggs, C. Yu, B. Fedoric, A. F. Lopez, S. J. Galli and M. A. Grimbaldeston J. Exp. Med., 2010, 207, 455–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. S. Gorman, N. M. Scott, D. H. Tan, C. E. Weeden, R. C. Tuckey, J. L. Bisley, M. A. Grimbaldeston and P. H. Hart PLoS One, 2012, 7, e46006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. A. Schwarz, F. Navid, T. Sparwasser, B. E. Clausen, and T. Schwarz J. Invest. Dermatol., 2012, 132, 2762–2769

    Article  CAS  PubMed  Google Scholar 

  175. M. Ahadi, M. Tabatabaeiyan, and K. Moazzami Endokrynol. Pol., 2011, 62, 134–137

    PubMed  Google Scholar 

  176. J. D. Cooper, D. J. Smyth, N. M. Walker, H. Stevens, O. S. Burren, C. Wallace, C. Greissl, E. Ramos-Lopez, E. Hypponen, D. B. Dunger, T. D. Spector, W. H. Ouwehand, T. J. Wang, K. Badenhoop and J. A. Todd Diabetes, 2011, 60, 1624–1631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. B. N. Frederiksen, M. Kroehl, T. E. Fingerlin, R. Wong, A. K. Steck, M. Rewers and J. M. Norris J. Clin. Endocrinol. Metab., 2013, 98, E1845–E1851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. S. U. Thorsen, H. B. Mortensen, B. Carstensen, M. Fenger, B. H. Thuesen, L. Husemoen, R. Bergholdt, C. Brorsson, F. Pociot, A. Linneberg, and J. Svensson Pediatr. Diabetes, 2014, 15, 416–421

    Article  CAS  PubMed  Google Scholar 

  179. A. G. Hussein, R. H. Mohamed and A. A. Alghobashy Cell. Immunol., 2012, 279, 42–45

    Article  CAS  PubMed  Google Scholar 

  180. D. Blanton, Z. Han, L. Bierschenk, M. V. Linga-Reddy, H. Wang, M. Clare-Salzler, M. Haller, D. Schatz, C. Myhr, J. X. She, C. Wasserfall, and M. Atkinson Diabetes, 2011, 60, 2566–2570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. R. Bailey, J. D. Cooper, L. Zeitels, D. J. Smyth, J. H. Yang, N. M. Walker, E. Hypponen, D. B. Dunger, E. Ramos-Lopez, K. Badenhoop, S. Nejentsev and J. A. Todd Diabetes, 2007, 56, 2616–2621

    Article  CAS  PubMed  Google Scholar 

  182. M. Fichna, M. Zurawek, D. Januszkiewicz-Lewandowska, P. Fichna, and J. Nowak Int. J. Immunogenet., 2010, 37, 367–372

    Article  CAS  PubMed  Google Scholar 

  183. E. R. Lopez, K. Regulla, M. A. Pani, M. Krause, K. H. Usadel, and K. Badenhoop J. Steroid Biochem. Mol. Biol., 2004, 89–90, 155–157

    Article  PubMed  CAS  Google Scholar 

  184. S. H. Abd-Allah, H. F. Pasha, H. A. Hagrass and A. A. Alghobashy Gene, 2014, 536, 430–434

    Article  CAS  PubMed  Google Scholar 

  185. D. Garcia, B. Angel, E. Carrasco, C. Albala, J. L. Santos and F. Perez-Bravo Diabetes Res. Clin. Pract., 2007, 77, 134–140

    Article  CAS  PubMed  Google Scholar 

  186. E. Capoluongo, D. Pitocco, P. Concolino, C. Santonocito, E. Di Stasio, G. d’Onofrio, A. Manto, B. Giardina, G. Ghirlanda, and F. Ameglio Clin. Biochem., 2006, 39, 888–892

    Article  CAS  PubMed  Google Scholar 

  187. M. C. Lemos, A. Fagulha, E. Coutinho, L. Gomes, M. Bastos, L. Barros, F. Carrilho, E. Geraldes, F. J. Regateiro, and M. Carvalheiro Hum. Immunol., 2008, 69, 134–138

    Article  CAS  PubMed  Google Scholar 

  188. E. O. Hamed, A. M. Abdel-Aal, A. K. Din and M. M. Atia Egyptian journal of immunology/Egyptian Association of Immunologists, 2013, 20, 1–10

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Telethon Kids Institute, 100 Roberts Road, Subiaco, Western Australia, 6008, Australia

    K. M. Miller, P. H. Hart & N. H. de Klerk

  2. Princess Margaret Hospital, Roberts Road, Subiaco, Western Australia, 6008, Australia

    E. A. Davis

  3. National Centre for Epidemiology and Population Health, The Australian National University, Canberra, 2600, Australia

    R. M. Lucas

Authors
  1. K. M. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. H. Hart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. H. de Klerk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. A. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. M. Lucas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. M. Miller.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial 3.0 License, which permits any non-commercial use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original authors and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc/3.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miller, K.M., Hart, P.H., de Klerk, N.H. et al. Are low sun exposure and/or vitamin D risk factors for type 1 diabetes?. Photochem Photobiol Sci 16, 381–398 (2017). https://doi.org/10.1039/c6pp00294c

Download citation

  • Received: 10 August 2016

  • Accepted: 27 November 2016

  • Published: 27 October 2020

  • Issue Date: March 2017

  • DOI: https://doi.org/10.1039/c6pp00294c

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

Use our pre-submission checklist

Avoid common mistakes on your manuscript.

Advertisement

Search

Navigation

  • Find a journal
  • Publish with us
  • Track your research

Discover content

  • Journals A-Z
  • Books A-Z

Publish with us

  • Publish your research
  • Open access publishing

Products and services

  • Our products
  • Librarians
  • Societies
  • Partners and advertisers

Our imprints

  • Springer
  • Nature Portfolio
  • BMC
  • Palgrave Macmillan
  • Apress
  • Your US state privacy rights
  • Accessibility statement
  • Terms and conditions
  • Privacy policy
  • Help and support

5.135.140.155

Not affiliated

Springer Nature

© 2024 Springer Nature