Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood
Open accessAbstract
OBJECTIVE: Early developmental adaptations in response to undernutrition may play an essential role in susceptibility to type 2 diabetes, particularly for those experiencing a "mismatched rich nutritional environment" in later life. We examined the associations of exposure to the Chinese famine (1959-1961) during fetal life and childhood with the risk of hyperglycemia and type 2 diabetes in adulthood. RESEARCH DESIGN AND METHODS: We used the data for 7,874 rural adults born between 1954 and 1964 in selected communities from the cross-sectional 2002 China National Nutrition and Health Survey. Hyperglycemia was defined as fasting plasma glucose ≥6.1 mmol/l and/or 2-h plasma glucose ≥7.8 mmol/l and/or a previous clinical diagnosis of type 2 diabetes. RESULTS: Prevalences of hyperglycemia among adults in nonexposed, fetal exposed, early-childhood, mid-childhood, and late-childhood exposed cohorts were 2.4%, 5.7%, 3.9%, 3.4%, and 5.9%, respectively. In severely affected famine areas, fetal-exposed subjects had an increased risk of hyperglycemia compared with nonexposed subjects (odds ratio = 3.92; 95% CI: 1.64-9.39; P = 0.002); this difference was not observed in less severely affected famine areas (odds ratio = 0.57; 95% CI: 0.25-1.31; P = 0.185). The odds ratios were significantly different between groups from the severe and less severe famine areas (P for interaction = 0.001). In severely affected famine areas, fetal-exposed subjects who followed an affluent/Western dietary pattern (odds ratios = 7.63; 95% CI: 2.41-24.1; P = 0.0005) or who had a higher economic status in later life experienced a substantially elevated risk of hyperglycemia (odds ratios = 6.20; 95% CI: 2.08-18.5; P = 0.001). CONCLUSIONS: Fetal exposure to the severe Chinese famine increases the risk of hyperglycemia in adulthood. This association appears to be exacerbated by a nutritionally rich environment in later life.
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Compared with the relatively nonexposed cohort, the ORs of hyperglycemia in the fetal-exposed cohort were 7.63 (95% CI 2.41-24.1, P = 0.0005) for those who had an affluent/Western dietary pattern, and 2.34 (95% CI 0.82-6.70, P = 0.112) for those with a traditional dietary pattern.
“Compared with the relatively nonexposed cohort, the ORs of hyperglycemia in the fetal-exposed cohort were 7.63 (95% CI 2.41–24.1, P = 0.0005) for those who had an affluent/Western dietary pattern, and 2.34 (95% CI 0.82–6.70, P = 0.112) for those with a traditional dietary pattern.”
From Globalization of Diabetes (2011) · cites this paper as [57]
In the Chinese National Nutrition and Health Survey, the prevalence of hyperglycemia was highest (18.9%) in fetal-exposed subjects who consumed an affluent/Western diet during adulthood.
“We found that the prevalence of hyperglycemia was highest (18.9%) in fetal-exposed subjects who consumed an affluent/Western diet during adulthood.”
From Globalization of Diabetes (2011) · cites this paper as [57]
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Cites
Effect of In Utero and Early-Life Conditions on Adult Health and Disease
Gluckman, P. D., Hanson, M. A., Cooper, C., & Thornburg, K. L. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0708473 · Cited by 3,898 · see citing works
Prevalence of Diabetes among Men and Women in China
Yang, W., Lu, J., Weng, J., Jia, W., Ji, L., Xiao, J., Shan, Z., Liu, J., Tian, H., Ji, Q., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa0908292 · Cited by 3,031 · see citing works
The thrifty phenotype hypothesis
Hales, C. N., & Barker, D. J. (2001) · British Medical Bulletin · doi:10.1093/bmb/60.1.5 · Cited by 2,749 · see citing works
Living with the Past: Evolution, Development, and Patterns of Disease
Gluckman, P. D., & Hanson, M. A. (2004) · Science · doi:10.1126/science.1095292 · Cited by 1,917 · see citing works
Glucose tolerance in adults after prenatal exposure to famine
Ravelli, A., van der Meulen, J., Michels, R., Osmond, C., Barker, D., Hales, C., & Bleker, O. (1998) · The Lancet · doi:10.1016/s0140-6736(97)07244-9 · Cited by 1,606 · see citing works
Birth Weight and Risk of Type 2 Diabetes
Whincup, P. H., Kaye, S. J., Owen, C. G., Huxley, R., Cook, D. G., Anazawa, S., Barrett-Connor, E. L., Bhargava, S. K., Birgisdóttir, B. E., Carlsson, S., et al. (2008) · JAMA · doi:10.1001/jama.2008.886 · Cited by 939 · see citing works
Prenatal stress, glucocorticoids and the programming of the brain
Welberg, L. A. M., & Seckl, J. R. (2001) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2001.00601.x · Cited by 928 · see citing works
Prenatal Stress, Glucocorticoids and the Programming of the Brain
Welberg, L., & Seckl, J. R. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00601.x · Cited by 922 · see citing works
Rates of Adult Schizophrenia Following Prenatal Exposure to the Chinese Famine of 1959-1961
Clair, D. S. (2005) · JAMA · doi:10.1001/jama.294.5.557 · Cited by 817 · see citing works
Neonatal anthropometry: the thin–fat Indian baby. The Pune Maternal Nutrition Study
Yajnik, C. S., Fall, C. H. D., Coyaji, K., Hirve, S. S., Rao, S. R., Barker, D. J. P., Joglekar, C. V., & Kellingray, S. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.802219 · Cited by 709 · see citing works
The long-term health and economic consequences of the 1959–1961 famine in China
Chen, Y., & Zhou, L. (2007) · Journal of Health Economics · doi:10.1016/j.jhealeco.2006.12.006 · Cited by 601 · see citing works
Stanner, S. A., Bulmer, K., Andrès, C., Lantseva, O. E., Borodina, V, Poteen, V. V., & Yudkin, J. S. (1997) · BMJ · doi:10.1136/bmj.315.7119.1342 · Cited by 545 · see citing works
Zhou, B. (2002) · PubMed · Cited by 526 · see citing works
Towards a new developmental synthesis: adaptive developmental plasticity and human disease
Gluckman, P. D., Hanson, M. A., Bateson, P., Beedle, A. S., Law, C., Bhutta, Z. A., Anokhin, K. V., Bougneres, P. F., Chandak, G. R., Dasgupta, P. S., et al. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60234-8 · Cited by 400 · see citing works
de Rooij, S. R., Painter, R. C., Roseboom, T. J., Phillips, D. I. W., Osmond, C., Barker, D. J. P., Tanck, M. W. T., Michels, R. P. J., Bossuyt, P. M., & Bleker, O. P. (2006) · Diabetologia · doi:10.1007/s00125-005-0136-9 · Cited by 237 · see citing works
Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat
Garofano, A., Czernichow, P., & Bréant, B. (1998) · Diabetologia · doi:10.1007/s001250051038 · Cited by 226 · see citing works
Puavilai, G., Chanprasertyotin, S., & Sriphrapradaeng, A. (1999) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(99)00008-x · Cited by 221 · see citing works
Intra-uterine programming of the endocrine pancreas
Fowden, A. L., & Hill, D. J. (2001) · British Medical Bulletin · doi:10.1093/bmb/60.1.123 · Cited by 189 · see citing works
Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period
Garofano, A., Czernichow, P., & Bréant, B. (1999) · Diabetologia · doi:10.1007/s001250051219 · Cited by 178 · see citing works
Famine and Overweight in China*
Luo, Z., Mu, R., & Zhang, X. (2006) · Review of Agricultural Economics · doi:10.1111/j.1467-9353.2006.00290.x · Cited by 160 · see citing works
Clark, P. M. (1998) · European Journal of Pediatrics · doi:10.1007/pl00014289 · Cited by 150 · see citing works
Wang, Y., Wang, X., Kong, Y., Zhang, J. H., & Zeng, Q. (2009) · Obesity · doi:10.1038/oby.2009.296 · Cited by 129 · see citing works
Dietary Patterns and Glucose Tolerance Abnormalities in Chinese Adults
He, Y., Ma, G., Zhai, F., Li, Y., Hu, Y., Feskens, E. J. M., & Yang, X. (2009) · Diabetes Care · doi:10.2337/dc09-0714 · Cited by 97 · see citing works
Self-citationImpact of famine during pregnancy and infancy on health in adulthood
Yang, Z., Zhao, W., Zhang, X., et al. (2008) · Obesity Reviews · doi:10.1111/j.1467-789x.2007.00447.x · Cited by 92 · see citing works
China's Agricultural Crisis and Famine of 1959–1961: A Survey and Comparison to Soviet Famines
Yang, D. T. (2008) · Comparative Economic Studies · doi:10.1057/ces.2008.4 · Cited by 69 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [27]State Statistical Bureau Quanguo Gesheng Zizhiqu Zhixiashi Lishi Tongji Ziliao Huibian, 1949–1989 (A Compilation of Historical Statistical Data of Provinces, Autonomous Regions, and Municipalities). Beijing China Statistical Press, 1990
Cited by
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Zheng, Y., Ley, S. H., & Hu, F. B. (2018) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2017.151 · Cited by 5,697 · see citing works
Self-citationThe worldwide epidemiology of type 2 diabetes mellitus—present and future perspectives
Chen, L., Magliano, D. J., & Zimmet, P. Z. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.183 · Cited by 2,227 · see citing works
Hu, F. B. (2011) · Diabetes Care · doi:10.2337/dc11-0442 · Cited by 1,954 · see citing works
Self-citationDiabetes: a 21st century challenge
Zimmet, P. Z., Magliano, D. J., Herman, W. H., & Shaw, J. E. (2014) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(13)70112-8 · Cited by 1,062 · see citing works
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Zimmet, P. Z. (2017) · Clinical Diabetes and Endocrinology · doi:10.1186/s40842-016-0039-3 · Cited by 338 · see citing works
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Barrès, R., & Zierath, J. R. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.87 · Cited by 198 · see citing works
The Elevated Susceptibility to Diabetes in India: An Evolutionary Perspective
Wells, J. C. K., Pomeroy, E., Walimbe, S. R., Popkin, B. M., & Yajnik, C. S. (2016) · Frontiers in Public Health · doi:10.3389/fpubh.2016.00145 · Cited by 155 · see citing works
Bouret, S., Levin, B. E., & Ozanne, S. E. (2015) · Physiological Reviews · doi:10.1152/physrev.00007.2014 · Cited by 157 · see citing works
Epidemiology of Diabetes—Status of a Pandemic and Issues Around Metabolic Surgery
Zimmet, P. Z., & Alberti, K. G. M. M. (2016) · Diabetes Care · doi:10.2337/dc16-0273 · Cited by 64 · see citing works
Childhood and adolescent exposures and the risk of endometriosis
Kvaskoff, M., Bijon, A., Clavel-Chapelon, F., Mesrine, S., & Boutron-Ruault, M.-C. (2013) · Epidemiology · doi:10.1097/ede.0b013e3182806445 · Cited by 47 · see citing works
- Authors
- Li, Y., He, Y., Qi, L., Jaddoe, V. W., Feskens, E. J. M., Yang, X., Ma, G., & Hu, F. B.
- Affiliations
- Harvard University (US)
- Chinese Center For Disease Control and Prevention (CN)
- Brigham and Women's Hospital (US)
- Wageningen University & Research (NL)
- Corresponding author
- Li, Yanping
- Ma, Guansheng
- Hu, Frank B.
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2010-07-09
- Volume
- 59
- Issue
- 10
- Pages
- 2400-2406
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- PMC
- PMC3279550
- OpenAlex
- W2144866168
- Cited by
- 384
- References
- 25
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 7 · 2023: 17 · 2022: 31 · 2021: 37 · 2020: 29 · 2019: 30 · 2018: 30 · 2017: 41 · 2016: 33 · 2015: 22 · 2014: 31 · 2013: 26 · 2012: 14
- FWCI
- 16.51
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Diabetes (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Socio-Environmental Systems Modeling (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- UNICEF
- Danone
- ZonMw (907.00303)
- Department of Global Health and Population, Harvard T.H. Chan School of Public Health
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Physiology › Dietary Effects on Health
- Keywords
- Chinese famine, fetal programming, developmental origins of health and disease, hyperglycemia, type 2 diabetes, malnutrition, child undernutrition, Western dietary pattern, economic status, fasting blood glucose, rural adults
- MeSH terms
- Adolescent, Adult, Blood Glucose, Child, Child, Preschool, China, Cross-Sectional Studies, Diabetes Mellitus, Type 2, Family Characteristics, Female, Health Surveys, Humans, Hyperglycemia, Pregnancy, Prenatal Exposure Delayed Effects, Rural Population, Starvation, Urban Population, Cohort Studies, Prevalence
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