Exposure to the Great Famine in Early Life and the Risk of Obesity in Adulthood: A Report Based on the China Health and Nutrition Survey
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Subjects
2.2. Measures
2.2.1. Exposure to Famine
2.2.2. Covariates
2.2.3. Outcomes
2.3. Statistical Analysis
3. Results
3.1. Characteristics of the Study Population
3.2. Age-Specific Body Measurements by Exposure to Famine
3.3. Associations of Famine Exposure with Body Measurements in Adulthood
3.4. Associations of Famine Exposure with Body Measurements at Specific Age Periods
3.5. Stratified Analysis of Associations between Famine Exposure and Body Measurements
3.6. Sensitivity Analysis
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Dai, H.; Alsalhe, T.A.; Chalghaf, N.; Riccò, M.; Bragazzi, N.L.; Wu, J. The global burden of disease attributable to high body mass index in 195 countries and territories, 1990–2017: An analysis of the Global Burden of Disease Study. PLoS Med. 2020, 17, e1003198. [Google Scholar] [CrossRef]
- Romieu, I.; On behalf of the IARC working group on Energy Balance and Obesity; Dossus, L.; Barquera, S.; Blottière, H.M.; Franks, P.W.; Gunter, M.; Hwalla, N.; Hursting, S.D.; Leitzmann, M.; et al. Energy balance and obesity: What are the main drivers? Cancer Causes Control. 2017, 28, 247–258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hanson, M.A.; Gluckman, P.D. Early developmental conditioning of later health and disease: Physiology or pathophysiology? Physiol. Rev. 2014, 94, 1027–1076. [Google Scholar] [CrossRef] [PubMed]
- Fernandez-Twinn, D.S.; Hjort, L.; Novakovic, B.; Ozanne, S.E.; Saffery, R. Intrauterine programming of obesity and type 2 diabetes. Diabetologia 2019, 62, 1789–1801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hales, C.N.; Barker, D.J.P. The thrifty phenotype hypothesis. Br. Med. Bull. 2001, 60, 5–20. [Google Scholar] [CrossRef] [Green Version]
- Jornayvaz, F.R.; Vollenweider, P.; Bochud, M.; Mooser, V.; Waeber, G.; Marques-Vidal, P. Low birth weight leads to obesity, diabetes and increased leptin levels in adults: The CoLaus study. Cardiovasc. Diabetol. 2016, 15, 73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roseboom, T.J.; Painter, R.C.; van Abeelen, A.F.; Veenendaal, M.V.; de Rooij, S.R. Hungry in the womb: What are the consequences? Lessons from the Dutch famine. Maturitas 2011, 70, 141–145. [Google Scholar] [CrossRef]
- Lumey, L.H.; Khalangot, M.D.; Vaiserman, A.M. Association between type 2 diabetes and prenatal exposure to the Ukraine famine of 1932–33: A retrospective cohort study. Lancet Diabetes Endocrinol. 2015, 3, 787–794. [Google Scholar] [CrossRef]
- Hult, M.; Tornhammar, P.; Ueda, P.; Chima, C.; Bonamy, A.-K.E.; Ozumba, B.; Norman, M. Hypertension, Diabetes and Overweight: Looming Legacies of the Biafran Famine. PLoS ONE 2010, 5, e13582. [Google Scholar] [CrossRef] [Green Version]
- Stein, A.D.; Kahn, H.S.; Rundle, A.; A Zybert, P.; Bruin, K.V.D.P.-D.; Lumey, L.H. Anthropometric measures in middle age after exposure to famine during gestation: Evidence from the Dutch famine. Am. J. Clin. Nutr. 2007, 85, 869–876. [Google Scholar] [CrossRef] [Green Version]
- Ravelli, A.C.; Van Der Meulen, J.H.; Osmond, C.; Barker, D.J.; Bleker, O.P. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am. J. Clin. Nutr. 1999, 70, 811–816. [Google Scholar] [CrossRef] [PubMed]
- Ravelli, G.-P.; Stein, Z.A.; Susser, M.W. Obesity in Young Men after Famine Exposure in Utero and Early Infancy. N. Engl. J. Med. 1976, 295, 349–353. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Lumey, L.H. 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, 1157–1170. [Google Scholar] [CrossRef]
- Wang, P.-X.; Wang, J.-J.; Lei, Y.-X.; Xiao, L.; Luo, Z.-C. Impact of Fetal and Infant Exposure to the Chinese Great Famine on the Risk of Hypertension in Adulthood. PLoS ONE 2012, 7, e49720. [Google Scholar] [CrossRef]
- 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, 1874–1878. [Google Scholar] [CrossRef] [Green Version]
- Liu, L.; Pang, Z.; Sun, J.; Xue, B.; Wang, S.; Ning, F.; Qiao, Q. Exposure to famine in early life and the risk of obesity in adulthood in Qingdao: Evidence from the 1959–1961 Chinese famine. Nutr. Metab. Cardiovasc. Dis. 2017, 27, 154–160. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Wang, X.; Kong, Y.; Zhang, J.H.; Zeng, Q. The Great Chinese Famine Leads to Shorter and Overweight Females in Chongqing Chinese Population After 50 Years. Obesity 2010, 18, 588–592. [Google Scholar] [CrossRef] [PubMed]
- Hu, X.; Wen, J.; Yu, W.; Yang, L.; Pan, W.; Xu, K.; Chen, X.; Li, Q.; Chen, G.; Gu, X. Associations of early-life exposure to famine with abdominal fat accumulation are independent of family history of diabetes and physical activity. Br. J. Nutr. 2021, 125, 943–950. [Google Scholar] [CrossRef] [PubMed]
- Chang, X.; Song, P.; Wang, M.; An, L. The Risks of Overweight, Obesity and Abdominal Obesity in Middle Age after Exposure to Famine in Early Life: Evidence from the China’s 1959–1961 Famine. J. Nutr. Health Aging 2018, 22, 1198–1204. [Google Scholar] [CrossRef]
- Huang, L.N.; Wang, H.J.; Wang, Z.H.; Ding, G.Q. Association between Chinese Famine Exposure and the Risk of Overweight/Obesity and Abdominal Obesity in Laterlife: A Cross-sectional Study. Biomed. Environ. Sci. 2020, 33, 133–137. [Google Scholar] [PubMed]
- Song, C.; Wang, M.; Chen, Z.; Yao, Y.; Feng, G.; Ma, Y.; Fan, J.; Liu, A. Fetal Exposure to Chinese Famine Increases Obesity Risk in Adulthood. Int. J. Environ. Res. Public Health 2020, 17, 3649. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Zhao, W.; Zhang, X.; Mu, R.; Zhai, Y.; Kong, L.; Chen, C. Impact of famine during pregnancy and infancy on health in adulthood. Obes. Rev. 2008, 9 (Suppl. S1), 95–99. [Google Scholar] [CrossRef]
- Liu, D.; Yu, D.-M.; Zhao, L.-Y.; Fang, H.-Y.; Zhang, J.; Wang, J.-Z.; Yang, Z.-Y.; Zhao, W.-H. Exposure to Famine during Early Life and Abdominal Obesity in Adulthood: Findings from the Great Chinese Famine during 1959–1961. Nutrients 2019, 11, 903. [Google Scholar] [CrossRef] [Green Version]
- Hidayat, K.; Du, X.; Shi, B.; Qin, L. 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. [Google Scholar] [CrossRef] [PubMed]
- Popkin, B.M.; Du, S.; Zhai, F.; Zhang, B. Cohort Profile: The China Health and Nutrition Survey—Monitoring and understanding socio-economic and health change in China, 1989–2011. Int. J. Epidemiol. 2010, 39, 1435–1440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jaacks, L.M.; Gordon-Larsen, P.; Mayer-Davis, E.J.; Adair, L.S.; Popkin, B. Age, Period and Cohort Effects on Adult Body Mass Index and Overweight from 1991 to 2009 in China: The China Health and Nutrition Survey. Int. J. Epidemiol. 2013, 42, 828–837. [Google Scholar] [CrossRef] [Green Version]
- Peng, X. Demographic Consequences of the Great Leap Forward in China’s Provinces. Popul. Dev. Rev. 1987, 13, 639–670. [Google Scholar] [CrossRef] [Green Version]
- Li, Q. Social Class in Current China: Measurement and Analysis; Beijing Norm. Univ. Press: Beijing, China, 2010; Volume 3, pp. 27–29. (In Chinese) [Google Scholar]
- Duncan, O.D. A Socioeconomic Index for All Occupations. In Occupations and Social Status; Reiss, J.A., Jr., Ed.; Free Press: New York, NY, USA, 1961; pp. 109–138. [Google Scholar]
- Patro, B.K.; Jeyashree, K.; Gupta, P.K. Kuppuswamy’s Socioeconomic Status Scale 2010—The Need for Periodic Revision. Indian J. Pediatr. 2012, 79, 395–396. [Google Scholar] [CrossRef]
- Popkin, B.M.; Paeratakul, S.; Ge, K.; Zhai, F. Body weight patterns among the Chinese: Results from the 1989 and 1991 China Health and Nutrition Surveys. Am. J. Public Health 1995, 85, 690–694. [Google Scholar] [CrossRef]
- World Health Organization. Waist Circumference and Waist-Hip Ratio: Report of a WHO Expert Consultation; World Health Organization: Geneva, Switzerland, 2008. [Google Scholar]
- National Institutes of Health. Managing Overweight and Obesity in Adults; National Institutes of Health: Bethesda, MD, USA, 2013. [Google Scholar]
- Roseboom, T.J.; van der Meulen, J.H.; Ravelli, A.C.; Osmond, C.; Barker, D.J.; Bleker, O.P. Effects of prenatal exposure to the Dutch famine on adult disease in later life: An overview. Mol. Cell. Endocrinol. 2001, 185, 93–98. [Google Scholar] [CrossRef]
- Tobi, E.W.; Lumey, L.H.; Talens, R.P.; Kremer, D.; Putter, H.; Stein, A.D.; Slagboom, P.E.; Heijmans, B.T. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum. Mol. Genet. 2009, 18, 4046–4053. [Google Scholar] [CrossRef]
- Luo, Z.; Mu, R.; Zhang, X.; Liu, G.G.; Zhang, S.; Zhang, Z. Famine and Overweight in China. Invest. Hum. Cap. Econ. Dev. China 2010, 28, 231–239. [Google Scholar]
- Prentice, A.M.; Moore, S.E. Early programming of adult diseases in resource poor countries. Arch. Dis. Child. 2005, 90, 429–432. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, R.; Duan, X.; Wu, Y.; Zhang, Q.; Chen, Y. Association of exposure to Chinese famine in early life with the incidence of hypertension in adulthood: A 22-year cohort study. Nutr. Metab. Cardiovasc. Dis. 2019, 29, 1237–1244. [Google Scholar] [CrossRef] [PubMed]
- Qi, H.; Hu, C.; Wang, S.; Zhang, Y.; Du, R.; Zhang, J.; Lin, L.; Wang, T.; Zhao, Z.; Li, M.; et al. Early life famine exposure, adulthood obesity patterns and the risk of nonalcoholic fatty liver disease. Liver Int. 2020, 40, 2694–2705. [Google Scholar] [CrossRef] [PubMed]
- Zhai, F.; Wang, H.; Du, S.; He, Y.; Wang, Z.; Ge, K.; Popkin, B.M. Prospective study on nutrition transition in China. Nutr. Rev. 2009, 67 (Suppl. S1), S56–S61. [Google Scholar] [CrossRef] [PubMed]
Unexposed (n = 8859) | Fetal-Exposed (n = 6203) | Childhood-Exposed (n = 7070) | p Values | |
---|---|---|---|---|
Men | ||||
No. of observations | 4503 | 3024 | 3602 | |
Age (years) | 38.2 ± 7.8 | 41.4 ± 7.3 | 44.0 ± 6.6 | <0.01 |
Areas of residence | 0.28 | |||
Urban area | 1445 (32.1) | 1011 (33.4) | 1211 (33.6) | |
Rural area | 3058 (67.9) | 2013 (66.6) | 2391 (66.4) | |
Famine severity of residence | <0.01 | |||
Less severe | 1525 (33.9) | 1166 (38.6) | 1189 (33.0) | |
More severe | 2978 (66.1) | 1858 (61.4) | 2413 (67.0) | |
SES at survey | <0.01 | |||
Lower class | 2029 (45.1) | 1154 (38.2) | 1777 (49.3) | |
Upper class | 2474 (54.9) | 1870 (61.8) | 1825 (50.7) | |
BMI (kg/m2) | 22.9 ± 3.6 | 23.3 ± 3.7 | 22.7 ± 3.4 | <0.01 |
WC (cm) | 81.2 ± 11.5 | 82.3 ± 11.2 | 80.8 ± 10.9 | <0.01 |
Overweight | 1154 (25.6) | 891 (29.5) | 834 (23.2) | <0.01 |
Central obesity | 912 (20.3) | 719 (23.8) | 645 (17.9) | <0.01 |
Women | ||||
No. of observations | 4356 | 3179 | 3468 | |
Age (years) | 39.0 ± 7.6 | 41.7 ± 7.4 | 44.6 ± 6.5 | <0.01 |
Residence | 0.94 | |||
Urban area | 1420 (32.6) | 1025 (32.2) | 1120 (32.3) | |
Rural area | 2936 (67.4) | 2154 (67.8) | 2348 (67.7) | |
Famine severity of residence | <0.01 | |||
Less severe | 1468 (33.7) | 1119 (35.2) | 1068 (30.8) | |
More severe | 2888 (66.3) | 2060 (64.8) | 2400 (69.2) | |
SES at survey | <0.01 | |||
Lower class | 2552 (58.6) | 1867 (58.7) | 2402 (69.3) | |
Upper class | 1804 (41.4) | 1312 (41.3) | 1066 (30.7) | |
BMI (kg/m2) | 23.0 ± 3.3 | 23.3 ± 3.5 | 23.3 ± 3.4 | <0.01 |
WC (cm) | 78.0 ± 10.0 | 78.9 ± 10.2 | 79.1 ± 10.1 | <0.01 |
Overweight | 1070 (24.6) | 911 (28.7) | 990 (28.6) | <0.01 |
Central obesity | 1641 (37.7) | 1326 (41.7) | 1426 (41.1) | <0.01 |
BMI (kg/m2) | WC (cm) | Overweight | Central Obesity | |||||
---|---|---|---|---|---|---|---|---|
Unadjusted β (95%CI) | Age-Adjusted β (95%CI) | Unadjusted β (95%CI) | Age-Adjusted β (95%CI) | Unadjusted OR (95%CI) | Age-Adjusted OR (95%CI) | Unadjusted OR (95%CI) | Age-Adjusted OR (95%CI) | |
Men | ||||||||
Fetal-exposed | 0.4 (0.1, 0.7) | −0.0 (−0.3, 0.3) | 1.2 (0.3, 2.0) | −0.5 (−1.3, 0.3) | 1.2 (1.1, 1.4) | 1.0 (0.8, 1.2) | 1.2 (1.1, 1.5) | 1.0 (0.9, 1.2) |
Childhood-exposed | −0.2 (−0.4, 0.1) | −0.9 (−1.1, −0.6) | −0.3 (−1.1, 0.4) | −3.2 (−4.0, −2.5) | 0.9 (0.7, 1.1) | 0.6 (0.5, 0.7) | 0.9 (0.7, 1.1) | 0.6 (0.5, 0.7) |
Women | ||||||||
Fetal-exposed | 0.3 (0.0, 0.6) | −0.0 (−0.3, 0.3) | 0.9 (0.1, 1.6) | −0.3 (−1.1, 0.5) | 1.2 (1.1, 1.5) | 1.0 (0.8, 1.3) | 1.2 (1.1, 1.4) | 1.0 (0.8, 1.1) |
Childhood-exposed | 0.3 (−0.0, 0.6) | −0.4 (−0.7, −0.1) | 1.1 (0.3, 1.8) | −1.3 (−2.0, −0.5) | 1.2 (1.1, 1.5) | 0.8 (0.7, 1.1) | 1.2 (1.1, 1.3) | 0.8 (0.7, 0.9) |
Men | Women | |||||||
---|---|---|---|---|---|---|---|---|
BMI (kg/m2) | WC (cm) | OverWeight | Central Obesity | BMI (kg/m2) | WC (cm) | OverWeight | Central Obesity | |
By SES | ||||||||
Lower Class | ||||||||
Fetal-exposed | 0.0 (−0.4, 0.4) | −0.7 (−1.8, 0.4) | 1.0 (0.7, 1.3) | 1.0 (0.7, 1.3) | −0.1 (−0.5, 0.3) | −0.4 (−1.4, 0.6) | 0.9 (0.7, 1.2) | 1.0 (0.8, 1.2) |
Childhood-exposed | −0.7 (−1.0, −0.4) | −3.0 (−4.0, −2.1) | 0.6 (0.4, 0.8) | 0.6 (0.4, 0.7) | −0.6 (−0.9, −0.2) | −1.4 (−2.4, −0.5) | 0.8 (0.6, 1.0) | 0.8 (0.7, 1.0) |
Upper Class | ||||||||
Fetal-exposed | −0.1 (−0.4, 0.3) | −0.5 (−1.4, 0.5) | 1.0 (0.8, 1.2) | 1.0 (0.8, 1.2) | 0.1 (−0.3, 0.4) | −0.2 (−1.2, 0.8) | 1.2 (0.9, 1.5) | 1.0 (0.8, 1.2) |
Childhood-exposed | −0.8 (−1.1, −0.4) | −2.7 (−3.7, −1.8) | 0.7 (0.6, 0.9) | 0.6 (0.5, 0.8) | −0.4 (−0.8, 0.0) | −1.5 (−2.5, −0.5) | 0.9 (0.7, 1.1) | 0.7 (0.5, 0.8) |
P for interaction | 0.93 | 0.86 | 0.77 | 0.89 | 0.76 | 0.51 | 0.12 | 0.10 |
By areas of residence | ||||||||
Urban areas | ||||||||
Fetal-exposed | −0.5 (−1.0, 0.0) | −1.6 (−3.0, −0.2) | 0.8 (0.6, 1.1) | 0.7 (0.5, 0.9) | −0.1 (−0.5, 0.4) | −0.6 (−1.8, 0.7) | 1.2 (0.8, 1.6) | 1.0 (0.8, 1.3) |
Childhood-exposed | −1.0 (−1.5, −0.5) | −3.3 (−4.7, −1.8) | 0.5 (0.4, 0.8) | 0.5 (0.3, 0.6) | −0.4 (−0.8, 0.1) | −0.6 (−1.8, 0.6) | 0.9 (0.7, 1.3) | 0.9 (0.7, 1.2) |
Rural areas | ||||||||
Fetal-exposed | 0.2 (−0.2, 0.5) | 0.1 (−0.9, 1.1) | 1.1 (0.9, 1.4) | 1.2 (0.9, 1.5) | −0.0 (−0.4, 0.4) | −0.2 (−1.1, 0.8) | 1.0 (0.8, 1.3) | 1.0 (0.8, 1.2) |
Childhood-exposed | −0.8 (−1.1, −0.5) | −3.3 (−4.2, −2.4) | 0.6 (0.5, 0.8) | 0.6 (0.5, 0.8) | −0.5 (−0.8, −0.1) | −1.6 (−2.6, −0.6) | 0.8 (0.6, 1.0) | 0.7 (0.6, 0.9) |
P for interaction | <0.01 | <0.01 | <0.01 | <0.01 | 0.78 | 0.07 | 0.70 | 0.36 |
By famine severity of residence | ||||||||
Less severe | ||||||||
Fetal-exposed | −0.1 (−0.5, 0.4) | −0.8 (−2.1, 0.5) | 1.0 (0.7, 1.4) | 1.0 (0.7, 1.4) | −0.7 (−1.2, −0.2) | −2.1 (−3.3, −0.8) | 0.7 (0.5, 0.9) | 0.7 (0.5, 0.9) |
Childhood-exposed | −0.8 (−1.3, −0.3) | −2.9 (−4.2, −1.5) | 0.7 (0.5, 0.9) | 0.6 (0.4, 0.8) | −0.4 (−0.9, 0.2) | −1.2 (−2.6, 0.2) | 0.9 (0.7, 1.3) | 0.7 (0.6, 1.0) |
More severe | ||||||||
Fetal-exposed | 0.1 (−0.3, 0.4) | −0.1 (−1.2, 0.9) | 1.0 (0.8, 1.3) | 1.0 (0.8, 1.2) | 0.3 (−0.1, 0.7) | 0.7 (−0.3, 1.6) | 1.3 (0.9, 1.6) | 1.2 (0.9, 1.4) |
Childhood-exposed | −0.9 (−1.2, −0.6) | −3.5 (−4.4, −2.5) | 0.6 (0.5, 0.7) | 0.5 (0.4, 0.7) | −0.5 (−0.9, −0.2) | −1.4 (−2.3, −0.4) | 0.8 (0.6, 0.9) | 0.8 (0.7, 0.9) |
P for interaction | 0.36 | 0.03 | 0.69 | 0.98 | <0.01 | <0.01 | <0.01 | <0.01 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Jiang, H.; Yu, Y.; Li, L.; Xu, W. Exposure to the Great Famine in Early Life and the Risk of Obesity in Adulthood: A Report Based on the China Health and Nutrition Survey. Nutrients 2021, 13, 1285. https://doi.org/10.3390/nu13041285
Jiang H, Yu Y, Li L, Xu W. Exposure to the Great Famine in Early Life and the Risk of Obesity in Adulthood: A Report Based on the China Health and Nutrition Survey. Nutrients. 2021; 13(4):1285. https://doi.org/10.3390/nu13041285
Chicago/Turabian StyleJiang, Huiru, Yongfu Yu, Leah Li, and Wanghong Xu. 2021. "Exposure to the Great Famine in Early Life and the Risk of Obesity in Adulthood: A Report Based on the China Health and Nutrition Survey" Nutrients 13, no. 4: 1285. https://doi.org/10.3390/nu13041285
APA StyleJiang, H., Yu, Y., Li, L., & Xu, W. (2021). Exposure to the Great Famine in Early Life and the Risk of Obesity in Adulthood: A Report Based on the China Health and Nutrition Survey. Nutrients, 13(4), 1285. https://doi.org/10.3390/nu13041285