Exposure to the Chinese famine of 1959-61 in early life and long-term health conditions: A systematic review and meta-analysis

International Journal of Epidemiology

Volumn 46, Issue 4, 2017, Pages 1157-1170

  Li, Chihua ^a   Lumey, L H ^a  

^a Columbia University ^*  (United States)

Author keywords

BMI; Delayed effects; Great Leap Forward Famine; Long term health; Prenatal exposure; Type 2 diabetes

Indexed keywords

BODY MASS; CONFIDENCE INTERVAL; DIABETES; DISEASE INCIDENCE; DISEASE SEVERITY; FAMINE; HYPERTENSION; LITERATURE REVIEW; META-ANALYSIS; MORTALITY; PUBLIC HEALTH;

ARTICLE; HEALTH STATUS; HUMAN; HUNGER; HYPERGLYCEMIA; HYPERTENSION; META ANALYSIS; METABOLIC SYNDROME X; MORTALITY; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; SCHIZOPHRENIA; SYSTEMATIC REVIEW; ASIAN CONTINENTAL ANCESTRY GROUP; CHINA; CHRONIC DISEASE; FEMALE; PREGNANCY; PRENATAL EXPOSURE; STARVATION;

CHINA;

ASIAN CONTINENTAL ANCESTRY GROUP; CHINA; CHRONIC DISEASE; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STARVATION;

EID: 85022171570     PISSN: 03005771     EISSN: 14643685     Source Type: Journal    
DOI: 10.1093/ije/dyx013     Document Type: Article

References (82)

1. Abegunde DO, Mathers CD, Adam T, Ortegon M, Strong K. The burden and costs of chronic diseases in low-income and middle-income countries. Lancet 2007;370:1929-38
2. Alwan A. Global Status Report on Noncommunicable Diseases 2010. Geneva: World Health Organization, 2011
3. Yang G, Wang Y, Zeng Yet al. Rapid health transition in China, 1990-2010:findings from the Global Burden of Disease Study 2010. Lancet 2013;381:1987-2015
4. Beaglehole R, Bonita R, Horton R et al. Priority actions for the non-communicable disease crisis. Lancet 2011;377:1438-47
5. Chang GH, Wen GJ. Communal dining and the Chinese famine of 1958-1961. Econ Dev Cult Change 1997;46:1-34
6. Peng X. Demographic consequences of the Great Leap Forward in China's provinces. Popul Dev Rev 1987;13:639-70
7. Ashton B, Hill K, Piazza A, Zeitz R. Famine in China, 1958-61. Popul Dev Rev 1984;10:613-45
8. Lin JY, Yang DT. Food availability, entitlements and the Chinese famine of 1959-61. Econ J 2000;110:136-58
9. Smil V. China's great famine: 40 years later. BMJ 1999;319:1619
10. Lumey LH, Stein AD, Susser E. Prenatal famine and adult health. Annu Rev Public Health 2011;32:237-62
11. Chmurzynska A. Fetal programming: link between early nutrition, DNA methylation, and complex diseases. Nutr Rev 2010;68:87-98
12. 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
13. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 2009;151:264-69
14. Gørgens T, Meng X, Vaithianathan R. Stunting and selection effects of famine: A case study of the Great Chinese Famine. J Dev Econ 2012;97:99-111
15. Chen Y, Zhou L. The long-term health and economic consequences of the 1959-1961 famine in China. J Health Econ 2007;26:659-81
16. Morgan S. The welfare consequences of the Great Leap Forward in China, 1959-1961: The stature of the survivor. Working paper. Department of Management, University of Melbourne, 2006
17. Stein Z, Susser M, Saenger G, Marolla F. Famine and Human Development: The Dutch Hunger Winter of 1944-1945. New York, NY: Oxford University Press, 1975
18. Van Wieringen J. Secular growth changes. In: Falkner F, Tanner J (eds). Human Growth: Postnatal Growth. New York, NY: Springer, 1978
19. Wells G, Shea B, O'Connell D et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. 2014, http://www.ohri.ca/programs/clinical_ epidemiology/oxford.asp3 February 2016, date last accessed
20. Yang Z, Zhao W, Zhang X et al. Impact of famine during pregnancy and infancy on health in adulthood. Obes Rev 2008;9:95-99
21. Wang Y, Wang X, Kong Y, Zhang JH, Zeng Q. The Great Chinese Famine leads to shorter and overweight females in Chongqing Chinese population after 50 years. Obesity 2010;18:588-92
22. Guan Y, Zhao Y, Li J, Li X, Hou J. Prevalence pilot study on population who was born in 1959-1961 in Chongqing. J Chongqing Med Univ 2009;34:1527-30
23. Zhao Y. Exposure to the 1959-1961 Chinese Famine in early life and the risk of chronic metabolic diseases in adulthhood Master's thesis. Department of Nutrition and Food, Anhui Medical University, 2013
24. Li Y, He Y, Qi L et al. Exposure to the Chinese famine in early life and the risk of hyperglycaemia and type 2 diabetes in adulthood. Diabetes 2010;59:2400-06
25. Liu D, Wang Y, Li T, Zhao Y. Attack rate of diabetes mellitus is significantly high in adults, born in 1960 (intermediate stage of famine times). J Chongqing Med Univ 2009;34:1712-14
26. Wang N, Wang X, Han B et al. Is exposure to famine in childhood and economic development in adulthood associated with diabetes? J Clin Endocrinol Metab 2015;100:4514-23
27. Xu H, Li L, Zhang Z, Liu J. Is natural experiment a cure? Reexamining the long-term health effects of China's 1959-1961 Famine. Soc Sci Med 2016;148:110-22
28. Zhang Z, Liu D. Diabetes survey during adulthood among people born in famine years. The Twelfth National Conference of Behavioral Medicine of Chinese Medical Academy, Conference date: 15 October 2010. Hebei, China: Chinese Medical Association, 2010
29. Li Y, Han H, Chen S et al. Effects related to experiences of famine during early life on diabetes mellitus and impaired fasting glucose during adulthood. Chin J Epidemiol 2014;35:853-55
30. Li T, Liu D, Wang Y, Zhao Y, Guan Y. Hyperglycaemia survey during adulthood among people born in famine years. The Seventh National Conference of Maternal and Child Nutrition of Chinese Nutrition Society, Conference date: 11 October 2010. Nanjing, China: Chinese Nutrition Society, 2010
31. Chen H, Nembhard WN, Stockwell HG. Sex-specific effects of fetal exposure to the 1959-1961 Chinese famine on risk of adult hypertension. Matern Child Health J 2013;18:527-33
32. Huang C, Li Z, Wang M, Martorell R. Early life exposure to the 1959-1961 Chinese famine has long-term health consequences. J Nutr 2010;140:1874-78
33. Li Y, Jaddoe VW, Qi L et al. Exposure to the Chinese famine in early life and the risk of hypertension in adulthood. J Hypertens 2011;29:1085-92
34. Wang P, Wang J, Lei Y, Xiao L, Luo Z. Impact of fetal and infant exposure to the Chinese Great Famine on the risk of hypertension in adulthood. PLoS One 2012;7:e79420
35. Guan Y, Wang Y, Li T, Peng B, Zhao Y. The impact of malnutrition caused of famine on the adult metabolic syndrome. Life Sci Res 2009;13:505-11
36. Li Y, Jaddoe VW, Qi L et al. Exposure to the Chinese famine in early life and the risk of metabolic syndrome in adulthood. Diabetes Care 2011;34:1014-18
37. Wang N, Wang X, Li Q et al. The famine exposure in early life and metabolic syndrome in adulthood. Clin Nutr 2015, Nov 24. doi: 10.1016/j.clnu.2015.11.010. [Epub ahead of print.]
38. Zheng X, Wang Y, Ren Wet 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;66:231-36
39. St Clair D, Xu M, Wang P et al. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959-1961. JAMA 2005;294:557-62
40. Xu M, Sun W, Liu B et al. Prenatal malnutrition and adult schizophrenia: further evidence from the 1959-1961 Chinese famine. Schizophr Bull 2009:sbn168
41. Fleiss J. Review papers: The statistical basis of meta-analysis. Stat Methods Med Res 1993;2:121-45
42. Egger M, Davey Smith G, Schneider M, Minder C. Bias in metaanalysis detected by a simple, graphical test. BMJ 1997;315:629-34
43. Huang C, Guo C, Nichols C, Chen S, Martorell R. Elevated levels of protein in urine in adulthood after exposure to the Chinese famine of 1959-61 during gestation and the early postnatal period. Int J Epidemiol 2014;43:1806-14
44. Huang C, Phillips MR, Zhang Y et al. Malnutrition in early life and adult mental health: evidence from a natural experiment. Soc Sci Med 2013;97:259-66
45. Song S, Wang W, Hu P. Famine, death, and madness:schizophrenia in early adulthood after prenatal exposure to the Chinese Great Leap Forward Famine. Soc Sci Med 2009;68:1315-21
46. Fung W. Early childhood malnutrition and adult obesity:Evidence from the 1959-61 China famine. PhD thesis. Boston, MA. Department of Economics, Harvard University, 2009
47. Luo Z, Mu R, Zhang X. Famine and overweight in China. Appl Econ Perspect Policy 2006;28:296-304
48. Dali Q, Li H, Li F et al. Nutrition deficiency increases the risk of stomach cancer mortality. BMC Cancer 2012;12:1-12
49. Li J, Na L, Ma H et al. Multigenerational effects of parental prenatal exposure to famine on adult offspring cognitive function. Sci Rep 2015;5:13792
50. Chen J, Peng B, Tang L et al. Fetal and infant exposure to the Chinese famine increases the risk of fatty liver disease in Chongqing, China. J Gastroenterol Hepatol 2016;31:200-05
51. Kim S, Fleisher BM, Sun JY. The long-term health effects of fetal malnutrition: evidence from the 1959-1961 China Great Leap Forward Famine. Health Econ 2016, Aug 19. doi: 10.1002/ hec.3397. [Epub ahead of print.]
52. Shi Z, Zhang C, Zhou M, Zhen S, Taylor AW. Exposure to the Chinese famine in early life and the risk of anaemia in adulthood. BMC Public Health 2013;13:904
53. Zhou L, Corruccini RS. Enamel hypoplasias related to famine stress in living Chinese. Am J Hum Biol 1998;10:723-33
54. Li Y, Shen Y, Ye K et al. Association between early life exposure to famine and damaging the liver and kidney function. Chin J Epidemiol 2014;35:848-51
55. Li Y, Zhu L, Wang J et al. The effects of exposure to the famine during early life with elevated resting heart rate in the adult. Chin J Prev Med 2015;49:600-04
56. Ma G. Long-term impact of the Chinese Famine on health: evidence from CHARLS and county-level death rate records.World Econ 2011;4:104-23
57. Zhang J, Li Y, Li L, Li X. The effect of the famine exposure in early life of the 50-year-old adult on the levels of body fat and blood glucose. J Bengbu Med School 2014;39:99-102
58. Reynolds K, Gu D, Whelton PK et al. Prevalence and risk factors of overweight and obesity in China. Obesity (Silver Spring) 2007;15:10-18
59. Gu D, Reynolds K, Wu X et al. Prevalence, awareness, treatment, and control of hypertension in China. J Hypertens 2002;40:920-27
60. Gu D, Reynolds K, Wu X et al. Prevalence of the metabolic syndrome and overweight among adults in China. Lancet 2005;365:1398-405
61. Yang W, Lu J, Weng J et al. Prevalence of diabetes among men and women in China. N Engl J Med 2010;362:1090-101
62. Li Y, Hu F, Ma G. Early life famine exposure and chronic diseases in China. In: Lumey L, Vaiserman A (eds). Early Life Nutrition, Adult Health and Development. New York, NY: Nova Science, 2013
63. Garnaut A. The geography of the Great Leap famine. Modern China 2014;40:315-48
64. Huang C, Li Z, Venkat Narayan K, Williamson D, Martorell R. Bigger babies born to women survivors of the 1959-1961 Chinese famine: a puzzle due to survival selection? J Dev Orig Health Dis 2010;1:412-18
65. Susser E, St Clair D. Prenatal famine and adult mental illness: interpreting concordant and discordant results from the Dutch and Chinese Famines. Soc Sci Med 2013;97:325-30
66. Xu Y, Wang L, He J et al. Prevalence and control of diabetes in Chinese adults. JAMA 2013;310:948-59
67. Yuan X, Liu T, Wu L, Zou Z-Y, Li C. Validity of self-reported diabetes among middle-aged and older Chinese adults: the China Health and Retirement Longitudinal Study. BMJ Open 2015;5:e006633
68. Zhao Y, Crimmins EM, Hu P et al. Prevalence, diagnosis, and management of diabetes mellitus among older Chinese: results from the China Health and Retirement Longitudinal Study. Int J Public Health 2016;61:347-56
69. Mu R, Zhang X. Gender Difference in the Long-term Impact of Famine. Washington, DC: Intl Food Policy Res Inst, 2008
70. Dickersin K. How important is publication bias? A synthesis of available data. AIDS Educ Prev 1997;9:15-21
71. Sutton AJ, Duval S, Tweedie R, Abrams KR, Jones DR. Empirical assessment of effect of publication bias on meta-analyses. BMJ 2000;320:1574-77
72. Kicinski M. Publication bias in recent meta-analyses. PLoS One 2013;8:e81823
73. Song S. Mortality consequences of the 1959-1961 Great Leap Forward famine in China: Debilitation, selection, and mortality crossovers. Soc Sci Med 2010;71:551-58
74. Zhao Y, Hu Y, Smith JP, Strauss J, Yang G. Cohort profile: The China Health and Retirement Longitudinal Study (CHARLS). Int J Epidemiol 2014;43:61
75. Shen J. Changing patterns and determinants of interprovincial migration in China 1985-2000. Popul Space Place 2012;18:384-402
76. Hu X, Cook S, Salazar MA. Internal migration and health in China. Lancet;372:1717-19
77. Tao R. Hukou reform and social security for migrant workers in China. Labour Migration and Social Development in Contemporary China 200873-95
78. Lumey LH, Stein A, Kahn H. 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
79. Ravelli AC, van der Meulen JH, Michels R et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet 1998;351:173-77
80. Tabulation on the 2010 Population Census of the People's Republic of China. Beijing: National Bureau of Statistics of China, 2012
81. Susser E, St Clair D, He L. Latent effects of prenatal malnutrition on adult health. Ann N YAcad Sci 2008;1136:185-92
82. Chen Z, Chen J, Collins R et al. China Kadoorie Biobank of 0.5 million people: survey methods, baseline characteristics and long-term follow-up. Int J Epidemiol 2011;40:1652-66