Cardiovascular medicine
Coronary heart disease after prenatal exposure to the Dutch
famine, 1944-45
T J Rosebooma, J H P van der Meulena, C Osmonde, D J P Barkere, A C J Ravellia, J M Schroeder-Tankab, G A van Montfransb, R P J Michelsc, O P Blekerd
a Department of
Clinical Epidemiology and Biostatistics, Academic Medical Centre,
University of Amsterdam, PO Box 22700, 1100 DE Amsterdam, Netherlands, b Department of Cardiology, Academic Medical
Centre, University of Amsterdam, c Department of Internal Medicine,
Academic Medical Centre, University of Amsterdam, d Department of Obstetrics and Gynaecology,
Academic Medical Centre, University of Amsterdam, e MRC
Environmental Epidemiology Unit, University of Southampton,
Southampton, UK
Correspondence to: Dr Roseboom t.j.roseboom{at}amc.uva.nl
Accepted 12 September
2000
OBJECTIVE
To assess the effect of
prenatal exposure to maternal malnutrition on coronary heart disease in
people born around the time of the Dutch famine, 1944-45.
DESIGN
Historical cohort study.
SETTING
Community study.
PATIENTS
Singletons born alive
between November 1943 and February 1947 for whom detailed birth records
were available.
DESIGN
The prevalence of coronary
heart disease was compared between those exposed to famine in late
gestation (n = 120), in mid-gestation (n = 108), or in early
gestation (n = 68), and those born in the year before the famine or
those conceived in the year after the famine (non-exposed subjects,
n = 440).
MAIN OUTCOME MEASURES
Prevalence of
coronary heart disease, defined as the presence of angina pectoris
according to the Rose questionnaire, Q waves on the ECG, or a history
of coronary revascularisation.
RESULTS
The prevalence of coronary
heart disease was higher in those exposed in early gestation than in
non-exposed people (8.8% v 3.2%; odds ratio
adjusted for sex 3.0, 95% confidence interval (CI) 1.1 to 8.1). The
prevalence was not increased in those exposed in mid gestation (0.9%)
or late gestation (2.5%). People with coronary heart disease tended to
have lower birth weights (3215 g v 3352 g,
p = 0.13), and smaller head circumferences at birth (32.2 cm
v 32.8 cm, p = 0.05), but the effect of
exposure to famine in early gestation was independent of birth weight
(adjusted odds ratio 3.2, 95% CI 1.2 to 8.8).
CONCLUSIONS
Although the numbers are
very small, this is the first evidence suggesting that maternal
malnutrition during early gestation contributes to the occurrence of
coronary heart disease in the offspring.
Keywords: coronary heart disease; fetal origins hypothesis; maternal malnutrition
© 2000 by Heart
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