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Long-Term Effects Of The 1959-1961 China Famine: Mainland China and Hong Kong
Douglas Almond, Lena ...
The Great Chinese Famine Leads to Shorter and Overweight Females in Chongqing Chinese Population After 50 Years
Yonghong Wang1,*, Xiaolin Wang1, Yuhan Kong2, John H. Zhang3 andQing Zeng4
Article first published online: 6 SEP 2012
DOI: 10.1038/oby.2009.296
2010 North American Association for the Study of Obesity (NAASO)
Issue Obesity
Obesity
Volume 18, Issue 3, pages 588–592, March 2010
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Abstract
This study investigated a possible association between early nutritional status during the famine, and the risk of overweight and obesity in adulthood in Chongqing Chinese population. The body weight, height, and BMI data were obtained from records of population (17,023) that had annual physical evaluations in the Public Health Center (in our hospital). Subjects born during 1956–1964 were divided into three groups: toddler group, all subjects who were born 1–3 years before the famine (1956–1958); gestational group, who were born during the famine period (1959–1961), and control group, who were born after the famine (1962–1964). The body weight and BMI were significantly higher, but the body height was significantly lower in the toddler and gestational groups (P < 0.05) in the female population as compared to the control group. The odds ratio of being overweight in females is more pronounced in the toddler group (1.48 times, 95% confidence interval (CI): 1.288–1.689) than in the gestational group (1.26 times, 95% CI: 1.089–1.457). The odds ratio of being obese in females is significantly higher in the toddler group (1.46 times, 95% CI: 1.288–1.689) than the control group. For males, the famine had no impact at all on the adulthood body weight in males. The Great Chinese Famine that affected the Chongqing population during 1959–1961 leads to shorter and overweight females, and the former is a risk factor for increased BMI in Chongqing. Second, the famine seems to be producing shorter but slimmer males in Chongqing. Furthermore, toddler's and maternal's malnutrition during the famine had important late consequences on the health status.
Introduction
There are definite evidences that show the risk factors of many diseases of adulthood are associated with major natural and social events during childhood, especially for the metabolic syndrome, stroke, hypertension, type 2 diabetes, obesity, and cardiovascular disease (1). Therefore, a “critical period” hypothesis suggested that the environmental conditions experienced in utero and prenatal periods are important, and may have a lifelong effect on later body constitution and the tendency to become obese (2). The term fetal programming of adult disease describes the long-term effect of maternal nutritional status on the birth body size and proportion. For example, it was suggested that under adverse nutritional conditions, fetuses maintain head size at the expense of body size (“head sparing”). This has specific implications for the stratification of risk factors for the adulthood diseases (3).
The Great Chinese Famine occurred in 1959–1961 that resulted in the death and the malnutrition of millions of people. Chongqing is a region that was severely affected by the famine. This natural disaster, however, provided an opportunity to study the effect of malnutrition on the long-term body development after 50 years. Therefore, in this study, we analyzed a possible association of the famine and the pregnancies during that time on the adulthood body weight, height, and BMI in the Chongqing Chinese population.
Methods and Procedures
Data source
The data were collected from subjects for annual physical evaluations from 2006 to 2008 in the Public Health Center of the First Affiliated Hospital of Chongqing Medical University in Chongqing, China. The data were randomized by multistep cluster sampling methods. The variables on subjects selected for this study included age, gender, and health indexes, including body height and body weight.
All subjects were Chongqing residents (n = 17,023) who were born in the years from 1956 to 1964. The subjects were divided into three groups by the birth years: 1–3 years before the famine (1956–1958), three years during the famine (1959–1961), and 1–3 years after the famine (1962–1964), and categorized as toddler, gestational, and control groups, respectively (Table 1). In our preliminary analysis, there was a significant difference between genders, and therefore, the data were grouped by gender.
Table 1. Gender and birth-year distribution
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Overweight and obesity standards
Overweight and obesity are usually defined by an indirect measure of body fat and the BMI (weight (kg)/height (m2)). The World Health Organization defines overweight with a BMI of 25.0–29.9 and obesity with a BMI ≥30. In the obesity research, the standard formulation has differences because of various nationalities' characteristics. We adopted the definition of overweight and obesity recommended by the Chinese guideline for prevention and control of overweight and obesity in Chinese adults', where underweight is defined as BMI <18.5, normal as BMI 18.5–23.9, overweight as BMI 24–27.9, and obesity BMI ≥28 (ref. 4).
Statistical analysis
The analysis of variance was used to determine the difference in body weight, body height, and BMI values among the groups. Then prevalence of overweight and obesity in the three groups was calculated. The χ2 test method was used to calculate differences in overweight and obesity prevalence among the three groups. A logistical model was developed to determine the odds ratio of the impact of the year of birth in adults overweight and obesity. The SAS 9.1 statistical program (SAS Institute, Cary, NC) was used to analyze the data.
Results
The effects of the famine on body height
In female subjects, the famine during the toddler and gestational stages had significantly reduced the adulthood body height (P < 0.05 vs. control) (Figure 1a). During the toddler stage, the famine reduced the adulthood body heights in male subjects (P < 0.05 vs. control) (Figure 1b). During the gestational stage, the famine had no impact on the adulthood male body height.
image
Figure 1. Comparison of body height in (a) female subjects and (b) male subjects (M ± s.d.). *P < 0.05 vs. control group born in 1962–1964.
The effects of the famine on body weight
A significant increase in the body weight of the toddler and gestational stages was observed in female subjects during the famine (P < 0.05 vs. control) (Figure 2a). During the toddler stage, the famine somehow reduced the adulthood body weights of the male subjects (P < 0.05 vs. control) (Figure 2b). Again, the famine, during the gestational stage, had no impact on the adulthood male body weight.
image
Figure 2. Comparison of body weight in (a) female subjects and (b) male subjects (M ± s.d.). *P < 0.05 vs. control group born in 1962–1964.
The effects of the famine on adult BMI
The famine had significantly increased the BMI of the female subjects during the toddler and gestational stages (P < 0.05 vs. control) (Figure 3a). Even though a tendency of a low BMI by the famine was observed in the male subjects of the toddler group, no statistical significance was obtained (Figure 3b).
image
Figure 3. Comparison of BMI in (a) female subjects and (b) male subjects (M ± s.d.). *P < 0.05 vs. control group born in 1962–1964.
Chinese criteria for overweight and obesity
Reassessing the BMI using the criteria of overweight and obesity for Chinese, there was a significantly higher prevalence in overweight in females in the toddler group (1956–1958) and in the gestational group (1959–1961) (P < 0.05 vs. control group) but not in males (Table 2). In addition, there was higher prevalence of obesity of the toddler group in females (P < 0.05) (Table 3). Compared with females born in the control group (1962–1964), the odds ratio for overweight of the toddler (1956–1958) and of the gestational groups (1959–1961) was increased by 47.5% (95% confidence interval (CI) 1.288–1.689) and 26% (95% CI 1.089–1.457) respectively. The odds ratio of obesity was increased in the toddler group (1956–1958) by 46.1% (95% CI 1.083–1.970).
Table 2. Comparison of overweight prevalence
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Table 3. Comparison of obesity prevalence
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Discussion
The 1959–1961 Great Chinese Famine was a 3-year period of extreme food shortage, especially in Chongqing region. This disastrous famine, in humanitarian terms, however, offers a unique opportunity to study the long-term effects of a period of severe maternal malnutrition during toddler and gestational stages on the adulthood body weight and height at a half century later. In the present study, we have observed the following results. First, toddler's nutritional status is crucial for adulthood body height in both females and males. The effect of the famine on body height is more pronounced in the toddler stage than in the gestational stage in both genders. The female subjects, during the toddler or gestational famine periods, are shorter than the control subjects. The male subjects, during the toddler famine, are shorter than the gestational famine and control subjects. The famine in Chongqing in 1959–1961 somehow selectively affected the female fetus on adulthood body height but spared the male fetus. Second, the toddler's nutritional status is crucial for adulthood body weight, but the effect is gender dependent. The famine in Chongqing increased female body weight (overweight/obese) in adulthood in both toddler and gestational famine subjects when compared to control subjects. In toddler's period, the famine somehow decreased male body weight in adulthood but failed to affect the adulthood body weight in the gestational famine subjects. Third, the BMI in female subjects is consistent with the body height and weight values, and showed an increase in adulthood BMI of toddler and gestational famine subjects. No statistical significance was obtained for adult male BMI among groups due to the reverse trend in male adulthood: body height and weight of the toddler and gestational groups. These observations are partially consistent with reports from other countries (5).
There are two important features observed in this study. First, the malnutrition, during the toddler stage but not the gestational stage, is more important for the adulthood body height and weight especially in females. Severe malnutrition during toddler and gestational stages leads to shorter but overweight females in Chongqing region in China 50 years later. This short and round body figure is more pronounced in the toddlers who were born at 1–3 years before the famine (Figures 1a and 2a). The adulthood body weight and height values from the famine fetus females are lower than that of the toddler and control groups. This observation indicates that for females of the toddler stage, malnutrition is an extremely important risk factor for adulthood body height and weight, especially in determining overweight and obesity. The gestational nutrition is also important but to a lesser degree when compared to toddler stage nutrition. Second, the famine on male development produced surprising results on male development. The first and the most important observation from this study is that the famine, during gestational stage, failed to make any impact at all on the adulthood body weight and height. It seems that malnutrition during gestational stage failed to affect male development in Chongqing region. Another interesting observation is that the famine during the toddler stage affected male body development but in a reverse trend as compared to that of females. Malnutrition in the toddler stage reduced adulthood body height and weight in males. It seems that the famine produced shorter but slimmer males in Chongqing region after 50 years.
The prevalence of obesity and overweight has increased dramatically in the 20th century in both economically developed countries and developing countries. It is estimated that >1 billion adults worldwide are overweight (i.e., BMI of 25.0–29.9 kg/m2) and >300 million adults worldwide are obese (BMI ≥30.0 kg/m2) (refs. 6,7). Contemporary prevalence of adult obesity is very high in United States (33% in both genders), in oil-rich Arabian countries (30% in males, 40% in females), and in European Union (up to 25% in both genders). In China, adult male overweight status tripled and female overweight status doubled between 1989 and 2000. By 2004, nearly a quarter of all adults in China were overweight (8). Obesity is associated with increased risks of comorbidities such as type 2 diabetes, metabolic syndrome, hypertension, cardiovascular diseases, and osteoarthritis (9). The economic cost of four chronic diseases (hypertension, diabetes, cardiovascular disease, and stroke) attributable to overweight and obesity was estimated to take account of 3.2 and 3.7% of 2003 National Health Care Expenditure and National Health Service Expenditure in China, respectively (10).
Adulthood overweight is affected by the childhood nutrition. Maternal dietary manipulation in animal models produces small offspring that display shortened life span, obesity, hypertension, diabetes (11,12), and alterations in the hypothalamic–pituitary–adrenal axis (13). These observations suggest that the origin of disease in later life lies in impaired development in utero. The fetus' developing tissues may be permanently altered by a suboptimal availability of nutrients, possibly providing a survival advantage in the short term. These adaptations can have profound effects on health in later life, even when the dietary insult was of short duration and had no effect on birth weight (14). Although there is strong evidence from animal models that maternal nutritional status during pregnancy can induce permanent changes in the fetus, it is not clear how this might apply to human populations.
This study, using a unique population at about 50 years after the Great Chinese Famine in Chongqing region, reconfirmed studies of Dutch Famine: severe malnutrition affects adulthood body height and weight. Maternal malnutrition was associated with higher BMI and waist circumference in 50-year-old women during gestation. But BMI of males was not significantly affected by exposure to famine during any stage of pregnancy (15). Lumey (16) studied intergenerational effects of exposure to the famine and found that during the Dutch Famine, women who had experienced famine for the first 6 months in utero had slightly smaller babies than women who had not been exposed to famine in utero. In addition, this study demonstrated several features in the Chongqing Chinese population, especially the gender difference at 50 years after the famine. The Great Chinese Famine seems to be leading to shorter and rounder females but shorter and slimmer males in Chongqing regions. The nutrition at the toddler stage is extremely important for both males and females, but again, there are gender differences. Females obtained a shorter and rounder body (overweight or obese) but males obtained a shorter but slimmer body at 50 years later.
There are several issues that need to be considered in interpreting our findings, such as socioeconomic status, gender preference, health care, infant survival, and maternal constitution or fertility. Even though we studied a relatively large population and divided the analysis by gender, these issues are beyond the scope of this study and require additional investigations. Another potential weakness of this study is the use of normal population, selective subjects that were fit and had normal employment who came to this center for routine health checkup, which may lead to underestimation of the effect of famine on overweight and obesity. The subjects who were affected severely by the overweight and obesity may not hold their jobs and therefore were “excluded” from this investigation. Furthermore, the selection of working force introduces a potential bias because about 15% of females in Chongqing region are homemakers and they were “excluded” from this study. Finally, because this study targets 50-year-old population, the Chinese retirement age introduces another issue. In China, male retires after 60 years, whereas female retires after 50 years. Therefore, it is likely more females were retired and they were “excluded” from this study.
Nevertheless, malnutrition in the early life is an important issue to be addressed because of their implications of the origin of adult diseases. The Barker hypothesis, also referred to the “fetal origin” hypothesis, proposes that the alterations in fetal nutrition and endocrine status result in developmental adaptations that permanently change the body's structure, physiology and metabolism, thereby predisposing individuals to cardiovascular, metabolic, and endocrine disease in adult life (17,18,19). Childhood malnutrition is also relevant for infantile health, growth and development. The most cost-effective strategy to prevent adulthood hypertension, stroke, diabetes, and other metabolic disorders that may be originated in the early life is to improve women's nutrition before and during pregnancy, and childhood's nutrition. This study demonstrated that the toddler stage nutrition is extremely important, for females and males.
Acknowledgments
In this study, we thank all participants: the data collection team of the First Affiliated Hospital, Chongqing Medical University, Chongqing, China. Q.Z. had full access to all the data, and takes responsibility for the integrity of the data and the accuracy of the data analysis in the study.
Disclosure
The authors declared no conflict of interest.
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