Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Famine exposure in early life and type 2 diabetes in adulthood: findings from prospective studies in China

  • Feng Ning (Qingdao Centers for Disease Control and Prevention) ;
  • Jing Zhao (School of Public Health, Guangzhou Medical University) ;
  • Lei Zhang (Department of Endocrine and Diabetes, Weifang Medical College) ;
  • Weijing Wang (Department of Epidemiology and Health Statistics, Qingdao University Medical College) ;
  • Xiaohui Sun (Qingdao Centers for Disease Control and Prevention) ;
  • Xin Song (Qingdao Centers for Disease Control and Prevention) ;
  • Yanlei Zhang (Department of Public Health, University of Helsinki) ;
  • Hualei Xin (Qingdao Centers for Disease Control and Prevention) ;
  • Weiguo Gao (Department of Endocrine and Diabetes, Weifang Medical College) ;
  • Ruqin Gao (Qingdao Centers for Disease Control and Prevention) ;
  • Dongfeng Zhang (Department of Epidemiology and Health Statistics, Qingdao University Medical College) ;
  • Zengchang Pang (Qingdao Centers for Disease Control and Prevention)
  • Received : 2022.04.04
  • Accepted : 2023.01.09
  • Published : 2023.08.01
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Abstract

BACKGROUND/OBJECTIVES: This study examined the relationship between famine exposure in early life and the risk of type 2 diabetes in adulthood during the 1959-1961 Chinese Famine. SUBJECTS/METHODS: A total of 3,418 individuals aged 35-74 years free of diabetes from two studies in 2006 and 2009 were followed up prospectively in 2009 and 2012, respectively. Famine exposure was classified as unexposed (individuals born in 1962-1978), fetal exposed (individuals born in 1959-1961), child exposed (individuals born in 1949-1958), and adolescent/adult exposed (born in 1931-1948). A logistic regression model was used to assess the relationship between famine exposure and diabetes after adjustment for potential covariates. RESULTS: During a three-year follow-up, the age-adjusted incidence rates of type 2 diabetes were 5.7%, 14.5%, 12.7%, and 17.8% in unexposed, fetal-exposed, child-exposed, and adolescent/adult-exposed groups, respectively (P < 0.01). Relative to the unexposed group, the relative risks (95% confidence interval) for diabetes were 2.15 (1.29-3.60), 1.53 (0.93-2.51), and 1.65 (0.75-3.63) in the fetal-exposed, child-exposed, and adolescent/adult-exposed groups, after controlling for potential covariates. The interactions between famine exposure and obesity, education level, and family history of diabetes were not observed, except for the urbanization type. Individuals living in rural areas with fetal and childhood famine exposure were at a higher risk of type 2 diabetes, with relative risks of 8.79 (1.82-42.54) and 2.33 (1.17-4.65), respectively. CONCLUSIONS: These findings indicate that famine exposure in early life is an independent predictor of type 2 diabetes, particularly in women. Early identification and intervention may help prevent diabetes in later life.

Keywords

Acknowledgement

We would like to express our sincere thanks to the local research teams from Qingdao Centers for Disease Prevention and Control, and Qingdao Endocrine and Diabetes Hospital, Qingdao, China.

References

  1. Pan XR, Yang WY, Li GW, Liu J; National Diabetes Prevention and Control Cooperative Group. Prevalence of diabetes and its risk factors in China, 1994. Diabetes Care 1997;20:1664-9. https://doi.org/10.2337/diacare.20.11.1664
  2. Li Y, Teng D, Shi X, Qin G, Qin Y, Quan H, Shi B, Sun H, Ba J, Chen B, et al. Prevalence of diabetes recorded in mainland China using 2018 diagnostic criteria from the American Diabetes Association: national cross sectional study. BMJ 2020;369:m997.
  3. Hidayat K, Du X, Shi BM, Qin LQ. Foetal and childhood exposure to famine and the risks of cardiometabolic conditions in adulthood: a systematic review and meta-analysis of observational studies. Obes Rev 2020;21:e12981.
  4. Liu L, Wang W, Sun J, Pang Z. Association of famine exposure during early life with the risk of type 2 diabetes in adulthood: a meta-analysis. Eur J Nutr 2018;57:741-9. https://doi.org/10.1007/s00394-016-1363-1
  5. Xin X, Yao J, Yang F, Zhang D. Famine exposure during early life and risk of hypertension in adulthood: a meta-analysis. Crit Rev Food Sci Nutr 2017;6:1-8.
  6. Li C, Lumey LH. Exposure to the Chinese famine of 1959-61 in early life and long-term health conditions: a systematic review and meta-analysis. Int J Epidemiol 2017;46:1157-70. https://doi.org/10.1093/ije/dyx013
  7. Ning F, Ren J, Song X, Zhang D, Liu L, Zhang L, Sun J, Zhang D, Pang Z, Qiao Q, et al. Qiao Q on behalf of Qingdao Diabetes Prevention Program(2019) Famine exposure in early life and risk of metabolic syndrome in adulthood: Comparisons of different metabolic syndrome definitions. J Diabetes Res 2019;2019:7954856.
  8. Ning F, Zhang D, Xue B, Zhang L, Zhang J, Zhu Z, Zhang D, Gao R, Pang Z, Qiao Q, et al. Synergistic effects of depression and obesity on type 2 diabetes incidence in Chinese adults. J Diabetes 2020;12:142-50. https://doi.org/10.1111/1753-0407.12968
  9. Andersson T, Alfredsson L, Kallberg H, Zdravkovic S, Ahlbom A. Calculating measures of biological interaction. Eur J Epidemiol 2005;20:575-9. https://doi.org/10.1007/s10654-005-7835-x
  10. Li Y, Han H, Chen S, Lu Y, Zhu L, Wen W, Cui L, Wu S. Effects related to experiences of famine during early life on diabetes mellitus and impaired fasting glucose during adulthood. Zhonghua Liu Xing Bing Xue Za Zhi 2014;35:852-5.
  11. Bercovich E, Keinan-Boker L, Shasha SM. Long-term health effects in adults born during the Holocaust. Isr Med Assoc J 2014;16:203-7.
  12. Meng R, Lv J, Yu C, Guo Y, Bian Z, Yang L, Chen Y, Zhang H, Chen X, Chen J, et al. Prenatal famine exposure, adulthood obesity patterns and risk of type 2 diabetes. Int J Epidemiol 2018;47:399-408. https://doi.org/10.1093/ije/dyx228
  13. van Abeelen AF, Elias SG, Bossuyt PM, Grobbee DE, van der Schouw YT, Roseboom TJ, Uiterwaal CS. Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes 2012;61:2255-60. https://doi.org/10.2337/db11-1559
  14. Lumey LH, Khalangot MD, Vaiserman AM. Association between type 2 diabetes and prenatal exposure to the Ukraine famine of 1932-33: a retrospective cohort study. Lancet Diabetes Endocrinol 2015;3:787-94. https://doi.org/10.1016/S2213-8587(15)00279-X
  15. Zhou J, Zhang L, Xuan P, Fan Y, Yang L, Hu C, Bo Q, Wang G, Sheng J, Wang S. The relationship between famine exposure during early life and body mass index in adulthood: a systematic review and meta-analysis. PLoS One 2018;13:e0192212.
  16. Singh GM, Danaei G, Farzadfar F, Stevens GA, Woodward M, Wormser D, Kaptoge S, Whitlock G, Qiao Q, Lewington S, et al. The age-specific quantitative effects of metabolic risk factors on cardiovascular diseases and diabetes: a pooled analysis. PLoS One 2013;8:e65174.
  17. Shepherd PR, Crowther NJ, Desai M, Hales CN, Ozanne SE. Altered adipocyte properties in the offspring of protein malnourished rats. Br J Nutr 1997;78:121-9. https://doi.org/10.1079/BJN19970124
  18. Wang Z, Zou Z, Yang Z, Dong Y, Song J, Dong B, Ma J, Arnold L. The association between fetal-stage exposure to the China famine and risk of diabetes mellitus in adulthood: results from the China health and retirement longitudinal study. BMC Public Health 2018;18:1205.
  19. Kline J, Stein Z, Susser M. Conception to Birth: Epidemiology of Prenatal Development. New York (NY): Oxford University Press; 1989. 
  20. Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull 2001;60:5-20. https://doi.org/10.1093/bmb/60.1.5
  21. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, Slagboom PE, Heijmans BT. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 2009;18:4046-53. https://doi.org/10.1093/hmg/ddp353
  22. Tobi EW, Slieker RC, Luijk R, Dekkers KF, Stein AD, Xu KM, Slagboom PE, van Zwet EW, Lumey LH, Heijmans BT, et al. DNA methylation as a mediator of the association between prenatal adversity and risk factors for metabolic disease in adulthood. Sci Adv 2018;4:eaao4364.