Early life undernutrition and chronic diseases at older ages: The effects of the Dutch famine on cardiovascular diseases and diabetes
Highlights
► Older females exposed to a famine at ages 11–14 are more likely to have Diabetes. ► Older females exposed to a famine at ages 11–14 are more likely to have PAD. ► Adolescence may be a critical period in the etiology of Diabetes and PAD.
Introduction
Adverse nutritional conditions in utero and during infancy are positively associated with the development of cardiovascular and respiratory diseases, stroke, and diabetes mellitus at older ages (Kuh and Ben-Shlomo, 2004, Newnham and Ross, 2009). These observed relationships may be the result of direct effects as suggested by the Fetal Origins Hypothesis of diseases (Barker, 1992). Barker postulates that exposure to poor nutritional conditions in utero and/or during the first months of postnatal life leads to alterations in the development of vital organs, tissues and/or body systems. These alterations, though likely advantageous for the survival in the short-term, may increase the predisposition to chronic diseases at older ages. Following the theory of Barker (1992), most past research has focussed on the long-term consequences of prenatal exposure to undernutrition (Kuh & Ben-Shlomo, 2004). For that reason, evidence is scarce on the effects of nutritional conditions during infancy, childhood, pre-adolescence and adolescence on chronic diseases at older ages.
This study addresses the long-term effects of undernutrition during pregnancy and until 14 on the prevalence of cardiovascular diseases and diabetes mellitus (DM). The exposure to undernutrition is determined by the place of residence during the severe famine that parts of the Netherlands faced during the winter 1944–45 at the end of World War II. The study distinguishes two types of cardiovascular diseases: heart diseases and peripheral arterial diseases (PAD). Cardiovascular diseases are currently the leading causes of death and account for 30% of all deaths globally (American Heart Association, 2009). The world prevalence of DM among adults was about 7% in 2009. It is expected to increase by 20% in developed countries and by 69% in developing countries between 2010 and 2030 (Shaw, Sicree, & Zimmet, 2009). The findings of the study will help to understand the etiology of cardiovascular diseases and DM at older ages and might enhance the identification of high-risk groups, for example in developing countries facing severe food restrictions. Prevention programs that aim at reducing the prevalence of cardiovascular diseases and/or DM may then more specifically focus on these high-risk populations.
Section snippets
The Dutch famine
The Dutch famine provides a unique historical context for the study at hand. This is for three main reasons. First, the famine took place during a very well-defined time period, specifically from November 1944 until May 1945, at the end of World War II. In October 1944, the Germans, who occupied the Netherlands, prohibited all transport, including food, to the Western part of the country as a response to a railroad strike initiated by the Dutch government in exile. The food embargo was highly
Cardiovascular diseases
A large number of studies find increased risks of cardiovascular disease at older ages for those with lower birth weight, those with shorter stature or smaller head circumference at birth, and those whose placenta was disproportionally large (e.g. Barker, 1997; Eriksson, Forsen, Tuomilehto, Osmond, & Barker, 2001; Khan and Shearman, 2005, Victora et al., 2008). These studies use birth outcomes as a proxy for the nutritional conditions in utero. However, birth outcomes may depend on unobserved
Dataset and sample
The data for this study are derived from the Longitudinal Aging Study Amsterdam (LASA) (Deeg, van Tilburg, Smit, & de Leeuw, 2002). LASA constitutes a nationally representative cohort of 3107 Dutch older individuals sampled from municipal registries, with oversampling of men and older individuals, followed since 1992. Initial ages at baseline were 55–85 years. The sample was constructed so as to reflect the national distribution of urbanization and population density. All LASA respondents at
Descriptive analysis
Table 1 reports descriptive statistics on all included variables by gender. 81 respondents were in utero or under age 1 during the famine, 293 were aged 1–5 years, 244 were aged 6–10 years, and 181 were aged 11–14 years. 278 respondents were exposed to the Dutch famine and 521 were non-exposed. In 2005–06, 186, 68, and 91 individuals had a heart disease, PAD, and DM, respectively. Table 1 also shows that exposed males have significantly more DM, fewer siblings, have moved significantly less
Discussion
The study shows significant associations between exposure to undernutrition during adolescence and the presence of PAD and DM at ages 60–76 for females. These associations remain after controlling for variations in parental educational level, number of siblings, smoking behavior and waist circumference.
Conclusions
Our study shows significant associations of exposure to famine at adolescent ages for PAD and DM for females. Exposure to severe undernutrition at ages 11–14 is associated with a higher probability of developing DM and/or PAD at ages 60–76 for females. As such, our study suggests that adolescence is a critical period with respect to exposure to adverse (nutritional) conditions and that future research should take this into account. The findings of our study are relevant for example for girls
Acknowledgments
The Longitudinal Aging Study Amsterdam (LASA) is primarily supported by a long-term grant from the Dutch ministry of Health, Welfare and Sports.
References (66)
- et al.
The pathophysiology of cigarette smoking and cardiovascular diseases
Journal of the American College of Cardiology
(2004) - et al.
Cardiovascular disease and stress
Encyclopedia of Stress
(2007) - et al.
Attrition on the longitudinal aging study Amsterdam: the effect of differential inclusion in side studies
Journal of Clinical Epidemiology
(2002) Cultural problems of aging especially regarding gender and intergenerational equity
Social Science & Medicine
(1996)- et al.
Gender, social network and survival time - a 20-year study of the rural elderly
Archives of Gerontology and Geriatrics
(1995) - et al.
Self-reports and general practitioner information on the presence of chronic diseases in community dwelling elderly. A study on the accuracy of patients’ self-reports and on determinants of inaccuracy
Journal of Clinical Epidemiology
(1996) - et al.
Obesity and Cardiovascular diseases: risk factor, paradox, and impact of weight loss
Journal of the American College of Cardiology
(2009) - et al.
Early onset of coronary artery disease after prenatal exposure to the Dutch famine
American Journal of Clinical Nutrition
(2006) - et al.
Glucose tolerance in adults after prenatal exposure to famine
The Lancet
(1998) - et al.
The Dutch famine and its long-term consequences for adult health
Early Human Development
(2006)
Maternal and child undernutrition: consequences for adult health and human capital
The Lancet
Impact of childhood experience of famine on late life health
Journal of Nutrition, Health, and Aging
International cardiovascular disease statistics
The fetal and infant origins of adult disease
Fetal nutrition and cardiovascular disease in later life
The Dutch famine
Can the influence of childhood SES on men and women’s adult body mass be explained by adult SES or personality? Findings from a national sample
Health Psychology
Birth weight and adult hypertension, diabetes mellitus and obesity in US men
Circulation
The Netherlands during the Second World War: 1939–1945, part 10B, first half
Birth weight, body silhouette over the life course, and incident diabetes in 91,453 middle-aged women from the French Etude Epidémiologique de Femmes de la Mutuelle Générale de l’Education Nationale (E3N)
Cohort Diabetes Care
Impaired insulin secretion after prenatal exposure to the Dutch famine
Diabetes Care
Why life speeds up as you get older? How memory shapes our past
Long term consequences of the 1944–1945 Dutch famine on the insulin-like growth factor axis
International Journal of Cancer
Early growth and coronary heart disease in later life: longitudinal study
British Medical Journal
The fetal and childhood growth of persons who develop type 2 diabetes
Annals of Internal Medicine
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis
Diabetologia
Gender differences in the link between childhood socioeconomic conditions and heart attack risk in adulthood
Demography
The nutritional basis of the fetal origins of adult diseases
International Journal of Epidemiology
Cardiovascular disease in a cohort exposed to the 1940–45 Channel Islands occupation
BMC Public Health
Development of the endocrine pancreas
Reviews in Endocrine and Metabolic Disorders
Cohort profile: The Longitudinal Aging Study Amsterdam (LASA)
International Journal of Epidemiology
Hypertension, diabetes and overweigth: looming legacies of the Biafran famine
PloS One
Can obesity be a risk factor in elderly people?
Obesity Reviews
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