Famines in the Last 100 Years: Implications for Diabetes

Whincup PH, Kaye SJ, Owen CG, Huxley R, Cook DG, Anazawa S, et al. Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008;300(24):2886–97. Barker DJP. Fetal and infants origins of adult disease. 1st ed. London: British Medical Journal; 1992. Hales CN, Barker DJP. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35:595–601. Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305(5691):1733–6. Thurner S, Klimek P, Szell M, Duftschmid G, Endel G, Kautzky-Willer A, et al. Quantification of excess risk for diabetes for those born in times of hunger, in an entire population of a nation, across a century. Proc Natl Acad Sci U S A. 2013;110(12):4703–7. This publication shows an excess in diabetes among the birth years associated with three famine periods. It is an important study as the cohort used is very large, diabetes is based on use of medication and different periods of famine all show the increase in diabetes risk. http://www.britannica.com/EBchecked/topic/612921/Ukraine/275912/Industrialization-and-collectivization. Vaiserman AM, Khalangot ND, Pisaruk AV, Mekhova LV, Koliada AK, Kutsenko KI, et al. Predisposition to type II diabetes in Ukraine residents exposed to famine 1932–1933 during prenatal development. Adv Gerontol. 2010;23(4):588–92. Stanner SA, Bulmer K, Andres C, Lantseva OE, Borodina V, Poteen VV, et al. Does malnutrition in utero determine diabetes and coronary heart disease in adulthood? Results from the Leningrad siege study, a cross sectional study. BMJ. 1997;315:1342–9. Ellison GTH. The health in later life of Channel Islanders exposed to the 1940–1945 occupation and siege. In: Lumey LH, Vaiserman AM, editors. Early life nutrition and adult health and development. Nova Science Publishers, 2013: 77–108. Lumey LH, Stein AD, Kahn HS. Food restriction during gestation and impaired fasting glucose or glucose tolerance and type 2 diabetes mellitus in adulthood: evidence from the Dutch Hunger Winter Families Study. J Dev Orig Health Dis. 2009;1:S164. Ravelli ACJ, van der Meulen JHP, Michels RPJ, Osmond C, Barker DJP, Hales CN, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998;351:173–7. de Rooij SR, Painter RC, Roseboom TJ, Phillips DI, Osmond C, Barker DJ, et al. Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine. Diabetologia. 2006;49:637–43. de Rooij SR, Painter RC, Phillips DI, Osmond C, Michels RP, Godsland IF, et al. Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care. 2006;29(8):1897–901. de Rooij SR, Painter RC, Phillips DI, Osmond C, Tanck MW, Defesche JC, et al. The effects of the Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-gamma2 gene on glucose/insulin metabolism interact with prenatal exposure to famine. Diabetes Care. 2006;29(5):1052–7. van Hoek M, Langendonk JG, de Rooij SR, Sijbrands EJ, Roseboom TJ. Genetic variant in the IGF2BP2 gene may interact with fetal malnutrition to affect glucose metabolism. Diabetes. 2009;58(6):1440–4. Botden IP, Zillikens MC, de Rooij SR, Langendonk JG, Danser AH, Sijbrands EJ, et al. Variants in the SIRT1 gene may affect diabetes risk in interaction with prenatal exposure to famine. Diabetes Care. 2012;35(2):424–6. Portrait F, Teeuwiszen E, Deeg D. Early life undernutrition and chronic diseases at older ages: the effects of the Dutch famine on cardiovascular diseases and diabetes. Soc Sci Med. 2011;73(5):711–8. van Abeelen AF, Elias SG, Bossuyt PM, Grobbee DE, van der Schouw YT, Roseboom TJ, et al. Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes. 2012;61(9):2255–60. This study was the first to show, using individual famine exposure data, that a short period of famine during postnatal development increases the risk for type 2 diabetes in adulthood. Li Y, He Y, Qi L, Jaddoe VW, Feskens EJ, Yang X, et al. Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes. 2010;59(10):2400–6. This study showed an effect of prenatal famine exposure on fasting plasma glucose levels and the risk of hyperglycemia. Interestingly, the hyperglycemia risk was highest among the fetally-exposed subjects who followed an affluent or Western dietary pattern or who had a higher economic status in later life. Li Y, Jaddoe VW, Qi L, He Y, Wang D, Lai J, et al. Exposure to the Chinese famine in early life and the risk of metabolic syndrome in adulthood. Diabetes Care. 2011;34(4):1014–8. Zheng X, Wang Y, Ren W, Luo R, Zhang S, Zhang JH, et al. Risk of metabolic syndrome in adults exposed to the great Chinese famine during the fetal life and early childhood. Eur J Clin Nutr. 2012;66(2):231–6. Hult M, Tornhammar P, Ueda P, Chima C, Bonamy AK, Ozumba B, et al. Hypertension, diabetes and overweight: looming legacies of the Biafran famine. PLoS One. 2010;5(10):e13582. This publication is the first to show in an African population that famine in early life is associated with type 2 diabetes later on. The prevalence of diabetes in sub-Saharan Africa is increasing and fetal and infant undernutrition may be a significant contributor to this. Dahri S, Snoeck A, Reusens-Billen B, Remacle C, Hoet JJ. Islet function in offspring of mothers on low-protein diet during gestation. Diabetes. 1991;40:115–20. Petrik J, Reusens B, Arany E, Remacle C, Coelho C, Hoet JJ, et al. A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology. 1999;140(10):4861–73. Garofano A, Czernichow P, Breant B. Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia. 1999;42(6):711–8. Van Assche FA, Aerts L. The fetal endocrine pancreas. Contrib Gynecol Obstet. 1979;5:44–57. Stein AD, Kahn HS, Rundle A, Zybert PA, van der Pal-de B, Lumey L. Anthropometric measures in middle age after exposure to famine during gestation: evidence from the Dutch famine. Am J Clin Nutr. 2007;85(3):869–76. Ravelli ACJ, van der Meulen JHP, Osmond C, Barker DJP, Bleker OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. AJCN. 1999;70:811–6. Lussana F, Painter RC, Ocke MC, Buller HR, Bossuyt PM, Roseboom TJ. Prenatal exposure to the Dutch famine is associated with a preference for fatty foods and a more atherogenic lipid profile. Am J Clin Nutr. 2008;88(6):1648–52. Stein AD, Rundle A, Wada N, Goldbohm RA, Lumey LH. Associations of gestational exposure to famine with energy balance and macronutrient density of the diet at age 58 years differ according to the reference population used. J Nutr. 2009;139(8):1555–61. Gluckman PD, Hanson MA. The fetal matrix: evolution, development and disease. First editionth ed. Cambridge: Cambridge University Press; 2005. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr. 2007;97(3):435–9. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005;135(6):1382–6. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105(44):17046–9. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet. 2009;18(21):4046–53. http://www.thousanddays.org/about/ Godfrey KM, Haugen G, Kiserud T, Inskip HM, Cooper C, Harvey NC, et al. Fetal liver blood flow distribution: role in human developmental strategy to prioritize fat deposition versus brain development. PLoS One. 2012;7(8):e41759. van Ewijk RJ, Painter RC, Roseboom TJ. Associations of prenatal exposure to Ramadan with small stature and thinness in adulthood: results from a large Indonesian population-based study. Am J Epidemiol. 2013;177(8):729–36. This study importantly shows that it is not only famine that can affect later health. Prenatal exposure to Ramadan also seems to form a risk factor for adverse health in later life. Ayyavoo A, Derraik JG, Hofman PL, Biggs J, Bloomfield FH, Cormack BE, et al. Severe hyperemesis gravidarum is associated with reduced insulin sensitivity in the offspring in childhood. J Clin Endocrinol Metab. 2013;98(8):3263–8. In line with the van Ewijk publication, this study forms another example of harmful effects of prenatal undernourishment. Here it was shown that excessive vomiting during pregnancy is associated with reduced insulin sensitivity in the offspring. de Rooij SR, Painter RC, Holleman F, Bossuyt PM, Roseboom TJ. The metabolic syndrome in adults prenatally exposed to the Dutch famine. Am J Clin Nutr. 2007;86(4):1219–24.