Anthropometric measures in middle age after exposure to famine during gestation: Evidence from the Dutch famine

Abstract

Few studies in humans have related maternal undernutrition to the size of the adult offspring.
The objective was to assess whether reductions in food intake by pregnant women during the Dutch famine of 1944-1945 were related to offspring length, weight, and indexes of adiposity in middle age.
We recruited 1) exposed persons born in western Netherlands between January 1945 and March 1946 whose mothers experienced famine during or immediately preceding pregnancy, 2) unexposed persons born in the same 3 institutions during 1943 or 1947 whose mothers did not experience famine during this pregnancy, and 3) unexposed same-sex siblings of persons in series 1 or 2. Anthropometric measurements (n = 427 males and 529 females) were obtained between 2003 and 2005. We defined 4 windows of gestational exposure (by ordinal weeks 1-10, 11-20, 21-30, and 31 through delivery) on the basis of exposure to a ration of <900 kcal/d during the whole 10-wk interval.
Exposure to reduced rations was associated with increased weight and greater indexes of fat deposition at several tissue sites in women but not in men (P for interaction <0.01). Measures of length and linear proportion were not associated with exposure to famine.
Reduced food availability may lead to increased adiposity later in life in female offspring.

Full text

Anthropometric measures in middle age after exposure to famine
during gestation: evidence from the Dutch famine
1⫺4
Aryeh D Stein, Henry S Kahn, Andrew Rundle, Patricia A Zybert, Karin van der Pal– de Bruin, and LH Lumey
ABSTRACT
Background: Few studies in humans have related maternal under-
nutrition to the size of the adult offspring.
Objective: The objective was to assess whether reductions in food
intake by pregnant women during the Dutch famine of 1944 –1945
were related to offspring length, weight, and indexes of adiposity in
middle age.
Design: We recruited 1) exposed persons born in western Nether-
lands between January 1945 and March 1946 whose mothers expe-
rienced famine during or immediately preceding pregnancy, 2) un-
exposed persons born in the same 3 institutions during 1943 or 1947
whose mothers did not experience famine during this pregnancy, and
3) unexposed same-sex siblings of persons in series 1 or 2. Anthro-
pometric measurements (n ҃ 427 males and 529 females) were
obtained between 2003 and 2005. We defined 4 windows of gesta-
tional exposure (by ordinal weeks 1–10, 11–20, 21–30, and 31
through delivery) on the basis of exposure to a ration of 쏝900 kcal/d
during the whole 10-wk interval.
Results: Exposure to reduced rations was associated with increased
weight and greater indexes of fat deposition at several tissue sites in
women but not in men (P for interaction 쏝0.01). Measures of length
and linear proportion were not associated with exposure to famine.
Conclusion: Reduced food availability may lead to increased adi-
posity later in life in female offspring. Am J Clin Nutr 2007;85:
869 –76.
KEY WORDS Anthropometric measures, body composition,
body mass index, body size, famine, maternal and infant health,
Netherlands, nutrition, obesity
INTRODUCTION
Adult body mass is a function of height, girth, and tissue mass
and distribution. Each of these measures has independent asso-
ciations with risk of disease and may have specific associations
with early development. Attained height, which is inversely as-
sociated with risk of cardiovascular disease (1), is strongly as-
sociated with birth length (2). Variations in body proportions,
such as the ratio of the leg to trunk lengths, may have their origin
in childhood (3) and are independent predictors of the risk of later
morbidity and mortality (4). Little is known about the role, if any,
of prenatal nutrition in the ontogeny of body proportions.
Birth weight, especially when adjusted for birth length, is
positively associated with measures of body size in later life (2).
Even so, and despite the consistent association between adult
overweight and type 2 diabetes or cardiovascular disease (5), an
increased birth weight is also associated with a decreased risk of
major chronic diseases (6). An explanation for this apparent
paradox might come from information on the sources of variation
in size at birth (7), but few studies of humans can document the
complex relations extending from maternal nutrition through
fetal development and risk of adult disease.
The Dutch famine of 1944 –1945 provides a rare opportunity
to study the long-term consequences of maternal undernutrition
in defined stages of gestation (8, 9). The Dutch famine affected
the western Netherlands (10 –12). Official rations, which by the
end of the famine consisted almost exclusively of bread and
potatoes, fell below 900 kcal/d by 26 November 1944 and were
as low as 500 kcal/d by April 1945. The famine ceased immedi-
ately after liberation. This extraordinary period of deprivation
affected fertility, weight gain during pregnancy, maternal blood
pressure, and infant size at birth (13–15). The reduction in fer-
tility was greater among manual than among nonmanual occu-
pational classes (8). The decline in mean birth weight of 300 g
was restricted to exposure to maternal undernutrition during the
third trimester (16, 17).
An earlier investigation of Dutch men aged 19 y found a
doubling of the prevalence of overweight with maternal exposure
to famine in midgestation (18). A second study, with data col-
lected when the famine-exposed birth cohort was aged 50 y,
reported increased body mass index (BMI; in kg/m
2
) in women
(but not in men) who were exposed to famine in early gestation
(19). To date, no studies have reported on other anthropometric
indexes of adiposity after gestation during the Dutch famine. The
present study was conducted to replicate the earlier findings,
extend follow-up through age 59 y, and analyze a wider array of
measures of tissue distribution. We also accounted statistically
1
From the Rollins School of Public Health, Emory University, Atlanta,
GA (ADS); the Division of Diabetes Translation, Centers for Disease Control
and Prevention, Atlanta, GA (HSK); the Mailman School of Public Health,
Columbia University, New York, NY (AR, PAZ, and LHL); and TNO Qual-
ity of Life, Leiden, Netherlands (KvdP).
2
The findings and conclusions in this report are those of the authors and do
not necessarily represent the views of the Centers for Disease Control and
Prevention.
3
Supported by grant RO1 HL067914 (Principal Investigator: LHL), Na-
tional Institutes of Health, Bethesda, MD.
4
Address reprint requests to LH Lumey, Department of Epidemiology,
Mailman School of Public Health, 722 West 168th Street, New York, NY
10032. E-mail: lumey@columbia.edu.
Received July 6, 2006.
Accepted for publication October 12, 2006.
869Am J Clin Nutr 2007;85:869 –76. Printed in USA. © 2007 American Society for Nutrition
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for familial determinants of growth and tissue distribution by
including same-sex siblings as control subjects.
SUBJECTS AND METHODS
Population source and tracing
We identified 3307 live singleton births (probands) at 3 insti-
tutions in famine-exposed cities (midwifery training schools in
Amsterdam and Rotterdam and the university hospital in Leiden)
in 1945 and early 1946 (100% sample) and in 1943 and 1947 (the
first 30 births/mo across the 3 institutions). At the time of the
famine, a large majority of deliveries (욷70%) in the Netherlands
were scheduled to occur at home. The client mix at the 2 mid-
wifery training schools consisted of low-risk pregnancies of
women of lower socioeconomic status whose home environment
was unsuitable for delivery. The client mix in Leiden included
such deliveries as well as women with higher-risk pregnancies
identified during prenatal care and emergency admissions
after complications of home labor. We extracted personal
identifiers, including name and maternal address, birth
weight, and other information from the admission logs and
delivery progress charts.
To trace the adult offspring, we provided the names and ad-
dresses at birth of all 3307 persons to the population register in
the municipality of birth. Of these named persons, 308 (9.3%)
were reported to have died and 275 (8.3%) to have migrated. For
294 persons (8.9%) a current address could not be located, and
the population registry in Rotterdam declined to trace 130 per-
sons born out of wedlock. Thus, a current address was obtained
for 2300 persons (70% of the institutional birth cohort).
Recruitment and examination
Traced persons were mailed a letter of invitation signed by the
current director of the institution in which they were born, a
brochure describing the study, and a response card. We mailed
one reminder letter to nonresponders. Initially, our study design
called for the recruitment of same-sex sibling pairs; hence, the
lack of an available sibling was a reason for ineligibility. We
received some reply from 1767 persons, of whom 347 (19.6%)
expressed willingness to participate together with a sibling. Of
those who declined, 67% reported not having a same-sex sibling
available for study. To increase the overall number of partici-
pants, therefore, we attempted to enroll persons who had indi-
cated ineligibility because of the lack of an available sibling.
We conducted a telephone interview, which was followed by
a clinical examination at the Leiden University Medical Center.
Most of the clinical examinations were conducted within 6 wk of
the telephone interview. All study protocols were approved by
the human subjects committees of the participating institutions,
and participants provided verbal consent at the start of the tele-
phone interview and written informed consent at the start of the
clinical examination. We obtained anthropometric measurements
from 971 subjects (437 men and 534 women): 311 proband-sibling
pairs, 2 siblings whose matching proband did not complete the
clinical examination, and 347 additional probands.
Anthropometric measures
All anthropometric measures were obtained by experienced
research nurses, who were provided specific training in the meth-
ods by one of us (HSK); only trivial differences in means or in the
variability of measures across nurses were observed. Weight was
obtained to the nearest 100 g with the participant standing on a
portable digital scale (SECA, Hamburg, Germany). Standing
height was measured to the nearest 1 mm with a portable stadi-
ometer (SECA), and seated height was obtained to the nearest 1
mm with the participant seated on a hard stool of known height
with the use of the same stadiometer. Right arm length (tip of
acromion to the distal tip of the third metacarpal bone) and waist
(at level of iliac crests, intersection with midaxillary line), hip
(buttocks at the point of maximum extension), and right midthigh
(supine with hip flexed at 45 °, between lateral inguinal crease
and proximal patella) circumferences were obtained to the near-
est 1 mm with the use of a nonextensible measuring tape
(Hoechstmass, Sulzbach, Germany). The supine sagittal abdom-
inal diameter (SAD) at the level of the iliac crests was obtained
to the nearest 1 mm with a sliding-beam caliper (Holtain, Dyfed,
Wales, United Kingdom). Tricipital, subscapular, and anterior
midthigh skinfold thicknesses were obtained to the nearest 0.2
mm with calipers with a maximal spread of 40 mm (Holtain).
These calipers were calibrated daily. A single measurement was
taken for height and weight. Two measurements were taken for
other anthropometric outcomes, and the mean was used for the
analysis. To ensure independence of the replicate measures, all
markings of measurement points were erased before the second
measure was obtained. If the first 2 measurements were not
sufficiently close (arm length, waist circumference, midthigh
circumference 1.0 cm; sagittal abdominal diameter 0.5 cm; sub-
scapular or triceps skinfold thickness 2.0 mm) a third and fourth
measure were taken and the 3 measures closest together from the
4 available measures were averaged.
Derived measures
Trunk length was calculated by subtracting the height of the
stool from seated height, and leg length was obtained by sub-
tracting trunk length from standing height. As indexes of body
proportion, we computed the ratios of the right arm to leg lengths
and the leg to trunk lengths. We computed the BMI. As additional
indexes of mass distribution, we computed the ratios of waist-
to-hip circumference, waist-to-midthigh circumference, and
SAD-to-midthigh circumference. We excluded from the analysis
individuals for whom any of the above anthropometric measures
were missing (n ҃ 12), for whom the ratio of trunk to leg length
exceeded 1.10 (n ҃ 2), and one man with polio-related atrophy
of a lower limb; the analytic sample consisted of 956 subjects.
Because several of the participants had one or more skinfold
thicknesses that exceeded the capacity of the calipers, we cate-
gorized the skinfold thicknesses into empirical quartiles. We
then developed a 3-level indicator of the relative distribution of
subcutaneous fat between the triceps and subscapular regions by
cross-tabulating the quartile distributions for these 2 regions. We
coded this indicator as Ҁ1 if the triceps value was in a higher
quartile of the distribution than was the subscapular value, as ѿ1
if the reverse was true, and 0 if both were in the same quartile.
Categorizing exposure to famine
We defined the start of each gestation by the date of the moth-
er’s last menstrual period (LMP), as noted in the original prenatal
record, unless it was missing or the resulting gestational age was
implausible (12.4%). In these cases, we approximated the date of
LMP from the unambiguous date of birth and estimates of ges-
tational age recorded on the birth record or from a gestational age
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estimate based on sex- and parity-specific birth weights of sin-
gleton live births at the Amsterdam midwives school and the
University of Amsterdam Department of Obstetrics between
1931 and 1965 at each gestation between 24 and 46 wk (20).
We characterized exposure to famine during gestation by de-
termining the weeks after the LMP during which the mother was
exposed to an official ration of 쏝900 kcal/d (the 24 wk included
the period from 26 November 1944 to 12 May 1945). We defined
the mother as exposed in specific periods if gestational weeks
1–10, 11–20, 21–30, or 31 to delivery were entirely included in
this time window. Thus, pregnancies with an LMP between 26
November 1944 and 4 March 1945 (n ҃ 74) were considered
exposed in weeks 1–10, between 18 September 1944 and 24
December 1944 (n ҃ 124) exposed in weeks 11–20, between 10
July 1944 and 15 October 1944 (n ҃ 140) exposed between
weeks 21–30, and between 2 May 1944 and 24 August 1944
(n ҃ 128) exposed between week 31 and delivery. Because these
time windows overlap, the participants could be considered ex-
posed during one or (at most) two 10-wk periods; those exposed
in at least one 10-week period (n ҃ 350) were considered to have
some exposure to famine. In this formulation, the estimate for
the variable “any exposure to famine” is not necessarily an av-
erage of the estimates for the four 10-wk periods, because these
may have independent and additive or counteractive associa-
tions with adult size.
Statistical methods
We computed means and SDs or categorical distributions, as
appropriate. We developed independent linear regression mod-
els for all models that did not include skinfold thicknesses. Skin-
fold thicknesses and their ratios were analyzed by using logistic
regression, with the highest category compared against all others.
Because humans are sexually dimorphic and previous research
has identified associations of famine with body composition in
one or the other sex (18, 19), we tested for heterogeneity of
associations by sex using F tests. We considered a P value 쏝0.10
to indicate an interaction and conducted sex-stratified analyses
where indicated.
We considered a set of models and regressed each outcome
variable separately on exposure to famine. Exposure to famine
was characterized by using an indicator for any gestational ex-
posure, with the reference category being no exposure, and by
using the four 10-wk intervals described, which we entered as a
set of 4 indicator variables. We used the combined population of
control subjects (unexposed births in the 3 hospitals: n ҃ 296;
siblings of the birth series: n ҃ 310) as the reference, and we
adjusted for age at examination. We used the xtreg and xtlogit
commands in STATA 8 (Stata Corp, College Station, TX) to
control for clustering within families. We assessed whether as-
sociations with exposure to famine were mediated through birth
weight or length by entering these terms and comparing the
changes in coefficients. These analyses were run on the institu-
tional birth series alone (birth weight: n ҃ 297 men and 348
women; birth length: n ҃ 278 men and 325 women; we lacked
information on size at birth for the sibling control subjects).
Estimates of the effect of exposure to famine were similar in
models that included the birth series and those that included the
birth series and the siblings.
We examined whether measurement error in seated height
because of excess adiposity in the buttocks might affect relations
by adding hip circumference to the relevant models. In practice,
this adjustment had no effect on any observed associations (data
not shown), and models without this adjustment are presented.
Models for circumferences, the SAD, and their resulting ratio
measures included a term for standing height to account for
allometric scaling; we also tested whether these associations
were affected by body proportion by including a term for the
leg-to-trunk ratio. Although the outcome measures were gener-
ally associated with both height and the leg-to-trunk ratio, addi-
tion of these terms did not alter the observed associations be-
tween the measures and exposure to famine (data not shown), and
we present results without this adjustment. Models for indexes of
mass distribution included adjustment terms describing adult
measures that might be causally related to adiposity, including
smoking status, intake of alcohol, intake of energy as estimated
from a food-frequency questionnaire, physical activity level in
the year before the examination as assessed by the SQUASH
questionnaire (21), and, for women, parity. In practice, control
for these factors did not affect the estimates (data not shown). We
did not consider these variables relevant for analyses of lengths
and body proportion because these outcomes are established by
early adulthood.
RESULTS
Differences between traced and untraced persons
The proportion of participants identified as deceased was
highest among probands born in 1943 (10.4%) and lowest among
probands born in 1947 (6.0%). Status as an emigrant or other
reasons why a current address was not found did not differ by
year of birth or period of exposure to famine. When we compared
the birth records of participants traced to a current address with
those who had either died, emigrated, or had not been located we
found no clinically significant differences in mean birth weight
(3350 compared with 3314 g) or length (50.4 compared with
50.2 cm), placental weight (601 compared with 592 g), maternal
age at delivery (28.2 compared with 27.4 y), or birth order (2.3
compared with 2.3).
Differences between interviewed and noninterviewed
persons
Of the 2300 persons who were invited to join the study, we
found no significant differences between those interviewed to
those who were not interviewed in mean birth weight (3374
compared with 3339 g) or length (50.5 compared with 50.3 cm),
placental weight (600 compared with 601 g), maternal age at
delivery (28.6 compared with 28.1 y), or birth order (2.4 com-
pared with 2.2). The response to our invitation, however, was
lower for those born in 1947 (25%) than in all others (35%).
Eleven percent of those who were interviewed lived within 5 km
of the examination site compared with 10% of those who were
not interviewed, and 34% of those interviewed lived 쏜45 km
from the examination site compared with 29% of those who were
not interviewed.
Final sample for analysis
We analyzed anthropometric data (except for skinfold thick-
nesses) from 956 persons. On the basis of their behavior and
anthropometric measures, these persons appeared unremarkable
for Dutch populations of this age (Table 1 and Table 2).
ANTHROPOMETRIC MEASURES AFTER MATERNAL UNDERNUTRITION 871
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Exposure to famine and measures of length and body
proportions
There was no evidence of a statistical interaction by sex in the
association of maternal exposure to famine with measures of
offspring length or their ratios (data not shown). There was no
overall association between exposure to famine and these mea-
sures when famine was considered as a whole (Table 3); when
considered as 4 periods of gestation, the ratio of the arm to leg
lengths showed gestation-period—specific associations, which
increased (P 쏝 0.10) after exposure in weeks 21–30 and de-
creased (P 쏝 0.05) after exposure in weeks 31 through delivery.
Exposure to famine and indexes of mass and mass
distribution
Strong statistical evidence for interaction by sex in the asso-
ciation of any famine exposure was found for all indexes of mass
distribution (P for heterogeneity 쏝 0.001) except waist-to-hip
ratio. For men, no association between any exposure to famine
and any index was found, whether considered individually or
when the 4 periods were considered as a group (Table 4; P 쏜 0.10
for all). In contrast, all the indexes were elevated in women
exposed to famine (P 쏝 0.05 for all, except the waist-to-hip ratio,
for which P 쏝 0.10) (Table 5); when the 4 periods of exposure
were considered as a group, the associations were significant
(P 쏝 0.01) for all measures, except the ratios of the waist-to-hip
circumferences and waist to midthigh circumferences (P 쏜 0.05
for both). Inspection of the period-specific estimates suggested
similarities between men and women for the estimates for expo-
sure in gestational weeks 1–10 and substantial divergence be-
tween men and women in the estimates for exposures in later
10-wk periods.
Skinfold thicknesses
In sex-pooled analyses (Table 6), the odds of being in the
highest quartile of the subscapular skinfold thickness and the
ratio of the subscapular to tricipital skinfold thickness were mod-
estly elevated with any exposure to famine (P 쏝 0.10). The test
for interaction by sex was not significant (P 쏜 0.10 in age-
adjusted models) for any skinfold thickness. There was no strong
indication of association with specific periods of exposure to
famine.
Analyses on birth series alone
We repeated all analyses using the 645 participants with mea-
sures of birth weight and the 603 participants with measures of
birth length. Results were very consistent with those reported for
the whole sample (data not shown). In these groups, the results
did not change when birth weight or birth length were included
in the model (data not shown).
DISCUSSION
In a follow-up study of persons exposed during gestation to the
Dutch famine of 1944 –1945, we observed that maternal expo-
sure to acute famine is associated with increases in several in-
dexes of body mass and mass distribution among female off-
spring at age 59 y. We did not observe any strong independent
association of prenatal exposure to famine with adult lengths or
body proportions.
The circumstances of the Dutch famine provide a model to test
for isolated effects of undernutrition at defined stages of devel-
opment and do not speak to the situation in which inadequate
prenatal nutrition is followed by continued undernutrition, as
TABLE 1
Selected characteristics of Dutch men and women examined between 2003 and 2005
Exposed to famine during
gestation (n ҃ 350)
Time control subjects
1
(n ҃ 296)
Sibling control subjects
(n ҃ 310) P
2
Sex (% male) 45.7 46.3 41.9 NS
Age (y) 58.9 앐 0.49
3
58.8 앐 1.57 57.3 앐 6.30 쏝0.01
Birth weight (kg)
4
3.30 앐 0.51 3.45 앐 0.49 — 쏝0.01
Birth length (cm)
4
50.3 앐 2.3 50.8 앐 2.2 — 쏝0.05
Energy intake (kcal/d) 2247 앐 625 2209 앐 649 2163 앐 630 NS
Physical activity score
5
7230 앐 4268 7871 앐 4936 7182 앐 3720 NS
Current smoker (%) 25.5 24.0 22.3 NS
Alcohol consumption (%) NS
쏝1 drink/wk 20.1 25.0 26.5
1–7 drinks/wk 37.9 33.5 31.3
8–14 drinks/wk 16.9 22.0 19.3
15–21 drinks/wk 15.5 12.2 12.9
쏜21 drinks/wk 9.5 7.4 10.0
Number of children (%) NS
0 10.3 13.9 14.2
1 16.9 14.5 11.6
2 56.6 53.7 52.3
욷3 16.3 18.0 22.0
1
Born in the same institution and not exposed to famine during gestation.
2
ANOVA or chi-square test as appropriate for comparison between categories.
3
x៮ 앐 SD (all such values).
4
Birth series only; siblings excluded.
5
Calculated from intensity of activity by reported average duration and frequency.
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was until recently common in many developing countries. Ex-
posure to famine, as we defined it in relation to official rations, is
an ecologic measure of undernutrition; we lacked individual
dietary intake data. However, evidence of the severity of the
famine was abundant, including evidence that during the height
of the famine pregnant women actually lost weight over the second
half of their pregnancy (15). Thus, our data support the notion that
maternal undernutrition in gestation, if postnatal nutrition and in-
fections are not limiting, neither programs a person for an altered
trajectory of linear growth if it occurs in early pregnancy nor results
in unrecoverable deficits in attained length if it occurs later in ges-
tation. In women, however, the prenatal deprivation appears to have
been associated with increased weight in middle age, with more of
the increased mass deposited centrally.
Two earlier studies of persons exposed to the Dutch famine in
utero have yielded mixed results. Among men examined at age
18 y, the absolute risk of obesity (defined as 쏜120% of the ideal
weight for height according to the Metropolitan Life Insurance
Company tables) was elevated from 1.5% to 2.8% with exposure
in midgestation (18). Our study lacked the power to detect an
effect of that small a magnitude. A study similar in design to ours
found an elevated BMI in women aged 50 y whose mothers were
exposed to the famine early in gestation, but there was no asso-
ciation with other periods of exposure to famine or among men
(19). Our results are broadly consistent with that study insofar as
we also observed a marked difference in associations between
men and women, but we did not identify early gestation as being
the critical window for effects in adulthood. A third study of the
consequences of exposure to famine, conducted among survivors
of the siege of Leningrad, did not suggest any difference in BMI
between those born before the siege commenced, born during the
siege, or born in an area not subject to the siege (22). That study
was unable to assess the timing of exposure to maternal under-
nutrition because the Leningrad siege lasted 쏜2 y. All of the
earlier studies considered only weight and height; we examined
a wider range of anthropometric dimensions and indexes. We
observed some suggestion that the heterogeneity of associations
between famine exposure and adult body mass and mass distribution
between men and women is established only after the first 10-wk
period of gestation. This may reflect the increasing importance of
sex-specific growth factors in fetal development (23).
There is ongoing debate about the relative utility of the avail-
able indexes of body mass distribution in predicting risk for
chronic disease (24-26). Although BMI is widely used, it does
TABLE 2
Selected body measurements and ratios for Dutch men and women examined between 2003 and 2005, by famine exposure and sex
Men Women
Exposed to
famine during
gestation (n ҃ 160)
Time control
subjects
1
(n ҃ 137)
Sibling control
subjects
(n ҃ 130)
Exposed to famine
during gestation
(n ҃ 190)
Time control
subjects
1
(n ҃ 159)
Sibling control
subjects
(n ҃ 180)
Height (cm) 177.4 앐 6.2
2
178.3 앐 6.3 178.9 앐 5.7 165.4 앐 6.6 165.4 앐 6.3 166.5 앐 6.9
Trunk length (cm) 92.6 앐 3.2 93.0 앐 3.2 93.5 앐 3.2 87.0 앐 3.3 86.8 앐 3.1 87.4 앐 3.4
Leg length (cm) 84.7 앐 4.3 85.3 앐 4.2 85.5 앐 4.1 78.4 앐 4.2 78.6 앐 4.5 79.1 앐 4.6
Arm length (cm) 66.8 앐 3.3 67.0 앐 3.7 67.1 앐 2.9 61.6 앐 3.3 61.8 앐 3.4 62.3 앐 3.7
Ratio of arm to leg lengths
(҂ 100)
78.9 앐 3.1 78.6 앐 3.0 78.6 앐 3.0 78.6 앐 2.9 78.6 앐 2.5 78.8 앐 3.3
Ratio of leg to trunk lengths
(҂ 100)
91.5 앐 4.5 91.7 앐 4.2 91.5 앐 4.7 90.1 앐 4.2 90.7 앐 5.2 90.6 앐 4.8
Weight (kg) 87.6 앐 12.1 88.8 앐 13.4 86.0 앐 11.6 78.7 앐 14.9 73.6 앐 13.4 75.3 앐 14.1
Waist circumference (cm) 100.5 앐 10.1 101.4 앐 10.5 98.4 앐 9.1 99.0 앐 11.9 93.9 앐 11.1 94.7 앐 12.0
Hip circumference (cm) 102.7 앐 6.6 103.1 앐 6.9 101.0 앐 5.7 108.9 앐 12.4 104.3 앐 9.7 105.1 앐 10.0
Supine sagittal abdominal
diameter (cm)
23.8 앐 3.0 23.9 앐 3.3 23.1 앐 2.8 23.2 앐 3.7 21.6 앐 3.4 21.7 앐 3.5
BMI (kg/m
2
)
27.8 앐 3.6 27.9 앐 4.0 26.8 앐 3.3 28.8 앐 5.7 26.9 앐 4.5 27.1 앐 4.8
Midthigh circumference
(cm)
52.1 앐 3.8 52.5 앐 4.1 51.8 앐 4.0 53.4 앐 6.5 51.4 앐 5.3 52.5 앐 5.3
Ratio of waist to hip
circumferences (҂ 100)
97.7 앐 5.5 98.3 앐 5.5 97.3 앐 5.7 91.0 앐 5.4 89.9 앐 5.8 90.0 앐 6.0
Ratio of supine sagittal
abdominal diameter to
midthigh circumference
(҂ 100)
45.6 앐 4.8 45.5 앐 4.7 44.6 앐 5.0 43.4 앐 4.8 42.1 앐 4.8 41.4 앐 5.5
Ratio of waist to midthigh
circumferences (҂ 10)
19.3 앐 1.5 19.3 앐 1.5 19.0 앐 1.7 18.6 앐 1.7 18.3 앐 1.6 18.1 앐 1.9
Subscapular skinfold
thickness (mm)
3,4
21.0 앐 8.3 [151] 19.0 앐 10.3 [136] 18.7 앐 9.6 23.1 앐 12.0 [189] 20.6 앐 10.7 [151] 21.4 앐 12.0 [172]
Triceps skinfold thickness
(mm)
4
12.9 앐 4.3 13.0 앐 6.6 13.8 앐 7.1 23.2 앐 10.5 [185] 22.2 앐 8.6 [151] 22.9 앐 9.1 [172]
Anterior midthigh skinfold
thickness (mm)
4
14.2 앐 7.5 [145] 15.4 앐 12.1 [127] 15.4 앐 7.5 [118] 31.7 앐쏜16.1 [130]
5
27.4 앐 15.9 [105] 30.0 앐 14.1 [135]
1
Born in the same institution and not exposed to famine during gestation.
2
x៮ 앐 SD (all such values).
3
Sample sizes for skinfold thicknesses include subjects in whom skinfold thicknesses were measured but for whom the skinfold thickness exceeded the
caliper capacity.
4
All values are medians and interquartile intervals; n in brackets.
5
The 75th percentile for this group exceeded the maximum caliper capacity of 40 mm. The 25th percentile was 23.9 mm.
ANTHROPOMETRIC MEASURES AFTER MATERNAL UNDERNUTRITION 873
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not differentiate between lean and fat tissue. The ratio of the
subscapular and tricipital skinfold thicknesses, a widely used
index of the distribution of subcutaneous fat, rather than of in-
creased visceral fat, was only weakly associated in the present
study with exposure to famine. Similarly, the waist-to-hip ratio,
a presumed correlate of ischemic heart disease (27), was mod-
estly associated with exposure in our study. We found, however,
that exposure to the famine was associated among women with
an increased ratio of SAD to the midthigh circumference—an
alternative anthropometric correlate of ischemic heart disease
(28). To date, there have been suggestions that exposure to fam-
ine in specific periods of gestation is associated with impaired
glucose tolerance (29) and with prevalent coronary heart disease
(30), inconsistently associated with blood pressure (31, 32), and
TABLE 3
Association of exposure to the Dutch famine overall or in the specified period of gestation with adult measures of length and with indexes of proportion for
956 persons examined between 2003 and 2005
1
Period of gestational exposure
Overall
(n ҃ 350)
Weeks 1–10
(n ҃ 74)
Weeks 11–20
(n ҃ 124)
Weeks 21–30
(n ҃ 140)
Week 31 to delivery
(n ҃ 128)
P
2
Estimate 95% CI Estimate 95% CI Estimate 95% CI Estimate 95% CI Estimate 95% CI
Length
Height (cm) Ҁ0.39 Ҁ1.11, 0.33 Ҁ0.30 Ҁ1.72, 1.13 Ҁ0.35 Ҁ1.51, 0.82 Ҁ1.01 Ҁ2.13, 0.11 0.51 Ҁ0.62, 1.63 NS
Trunk (cm) Ҁ0.03 Ҁ0.41, 0.35 0.11 Ҁ0.62, 0.85 Ҁ0.12 Ҁ0.73, 0.49 Ҁ0.28 Ҁ0.87, 0.30 0.17 Ҁ0.41, 0.76 NS
Leg (cm) Ҁ0.40 Ҁ0.90, 0.10 Ҁ0.47 Ҁ1.45, 0.52 Ҁ0.26 Ҁ1.07, 0.55 Ҁ0.72 Ҁ1.50, 0.06 0.29 Ҁ0.49, 1.07 NS
Arm (cm) Ҁ0.23 Ҁ0.65, 0.19 Ҁ0.41 Ҁ1.21, 0.40 Ҁ0.13 Ҁ0.80, 0.54 Ҁ0.07 Ҁ0.71, 0.57 Ҁ0.13 Ҁ0.77, 0.51 NS
Indexes of proportion
Ratio of arm to leg
lengths (҂ 100)
0.10 Ҁ0.28, 0.49 0.07 Ҁ0.65, 0.79 0.26 Ҁ0.34, 0.87 0.58 0.00, 1.16 Ҁ0.65 Ҁ1.22, Ҁ0.08 쏝0.05
Ratio of leg to trunk
lengths (҂ 100)
Ҁ0.44 Ҁ1.00, 0.12 Ҁ0.75 Ҁ1.83, 0.34 Ҁ0.26 Ҁ1.16, 0.64 Ҁ0.53 Ҁ1.39, 0.34 0.30 Ҁ0.56, 1.17 NS
1
Values represent differences from control group (n ҃ 606). Estimates were obtained by linear regression and were adjusted for sex, age, and clustering
of siblings. Models for each specific 10-wk period of gestational exposure were also adjusted for exposure in overlapping 10-wk periods. Estimates for any
exposure may reflect additive effects of exposure in specific periods. Tests for interaction by sex were not significant (P 쏜 0.25 for each outcome).
2
Values reflect the overall test of association of all 4 periods of exposure considered as a group (Wald test, 4 df).
TABLE 4
Association of exposure to the Dutch famine overall or in the specified period of gestation with weight, circumferences, and indicators of body
composition in adulthood for 427 men measured between 2003 and 2005
1
Period of gestational exposure
Overall
(n ҃ 160)
Weeks 1–10
(n ҃ 35)
Weeks 11–20
(n ҃ 59)
Weeks 21–30
(n ҃ 69)
Week 31 to delivery
(n ҃ 59)
P
2
Estimate 95% CI Estimate 95% CI Estimate 95% CI Estimate 95% CI Estimate 95% CI
Weight and circumferences
Weight (kg) 0.98 Ҁ1.22, 3.18 3.37 Ҁ0.73, 7.46 Ҁ1.63 Ҁ5.19, 1.93 2.08 Ҁ1.31, 5.47 Ҁ1.17 Ҁ4.49, 2.16 NS
Waist circumference (cm) 0.51 Ҁ1.40, 2.42 1.82 Ҁ1.73, 5.37 Ҁ1.28 Ҁ4.37, 1.81 1.88 Ҁ1.06, 4.82 Ҁ0.37 Ҁ3.25, 2.51 NS
Hip circumference (cm) 0.73 Ҁ0.43, 1.90 1.94 Ҁ0.27, 4.15 Ҁ0.48 Ҁ2.38, 1.43 0.93 Ҁ0.89, 2.76 Ҁ0.43 Ҁ2.21, 1.36 NS
Supine sagittal abdominal
diameter (cm)
0.20 Ҁ0.38, 0.79 0.84 Ҁ0.26, 1.93 Ҁ0.42 Ҁ1.37, 0.54 0.37 Ҁ0.54, 1.28 0.01 Ҁ0.88, 0.90 NS
Midthigh circumference (cm) 0.11 Ҁ0.64, 0.87 1.04 Ҁ0.34, 2.42 0.22 Ҁ0.99, 1.43 Ҁ0.07 Ҁ1.22, 1.07 Ҁ0.73 Ҁ1.85, 0.40 NS
Indexes of mass distribution
BMI (kg/m
2
)
0.32 Ҁ0.37, 1.01 1.06 Ҁ0.23, 2.34 Ҁ0.49 Ҁ1.61, 0.63 0.66 Ҁ0.41, 1.72 Ҁ0.35 Ҁ1.40, 0.69 NS
Ratio of waist to hip
circumferences (҂ 100)
Ҁ0.27 Ҁ1.34, 0.80 0.01 Ҁ1.97, 1.98 Ҁ0.86 Ҁ2.59, 0.86 0.82 Ҁ0.82, 2.46 0.11 Ҁ1.50, 1.72 NS
Ratio of supine sagittal
abdominal diameter to
midthigh circumference
(҂ 100)
0.31 Ҁ0.61, 1.23 0.70 Ҁ1.00, 2.40 Ҁ0.86 Ҁ2.34, 0.62 0.66 Ҁ0.75, 2.06 0.76 Ҁ0.62, 2.14 NS
Ratio of waist to midthigh
circumferences (҂ 100)
0.50 Ҁ2.47, 3.47 Ҁ0.17 Ҁ5.63, 5.29 Ҁ2.91 Ҁ7.68, 1.86 3.43 Ҁ1.10, 7.96 2.20 Ҁ2.25, 6.64 NS
1
Values represent differences from control group (n ҃ 267). Estimates were obtained by linear regression and were adjusted for age, height, and clustering
of siblings. Estimates for specific 10-wk periods of gestational exposure were also adjusted for exposure in overlapping 10-wk periods. Estimates for any
exposure may reflect the additive effects of exposure in specific periods.
2
Values reflect the overall test of association of all 4 periods of exposure considered as a group (Wald test, 4 df).
874 STEIN ET AL
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not associated with overall mortality (33); all these conditions
have shown associations with adiposity. Thus, future research
needs to consider how differences in adiposity consequent to
exposure to famine during gestation, including differences in the
distribution of lean and adipose tissue throughout the body,
might mediate any effect of the famine on risk of disease.
It is possible that participation bias may have led to our find-
ings if heavy women with famine exposure were more likely to
TABLE 5
Association of exposure to the Dutch famine overall or in the specified period of gestation with weight, circumferences, and indexes of adiposity in
adulthood for 529 women measured between 2003 and 2005
1
Period of gestational exposure
Overall
(n ҃ 190)
Weeks 1–10
(n ҃ 39)
Weeks 11–20
(n ҃ 65)
Weeks 21–30
(n ҃ 71)
Week 31 to delivery
(n ҃ 69)
P
2
Estimate 95% CI Estimate 95% CI Estimate 95% CI Estimate 95% CI Estimate 95% CI
Weight and circumferences
Weight (kg) 4.83
3
2.51, 7.14 3.98 Ҁ0.53, 8.48 3.71 0.04, 7.39 3.53 0.02, 7.05 2.75 Ҁ0.77, 6.26 쏝0.01
Waist circumference (cm) 4.69
3
2.66, 6.72 1.96 Ҁ1.93, 5.85 2.83 0.64, 7.02 3.88 0.83, 6.93 2.50 Ҁ0.53, 5.53 쏝0.01
Hip circumference (cm) 4.37
3
2.58, 6.15 2.86 Ҁ0.66, 6.38 3.81 0.96, 6.66 3.27 0.54, 6.00 2.56 Ҁ0.18, 5.30 쏝0.01
Supine sagittal abdominal
diameter (cm)
1.52
3
0.91, 2.13 1.00 Ҁ0.18, 2.18 1.13 0.17, 2.10 0.84 Ҁ0.08, 1.77 1.34 0.42, 2.26 쏝0.01
Midthigh circumference
(cm)
1.61
3
0.65, 2.57 1.01 Ҁ0.86, 2.88 1.40 Ҁ0.12, 2.92 1.64 0.18, 3.09 0.56 Ҁ0.90, 2.01 쏝0.01
Indexes of mass distribution
BMI (kg/m
2
)
1.85
3
1.01, 2.69 1.44 Ҁ0.21, 3.09 1.45 0.11, 2.80 1.34 0.06, 2.62 1.08 Ҁ0.20, 2.37 쏝0.01
Ratio of waist to hip
circumferences (҂ 100)
0.89
4
Ҁ0.15, 1.83 0.09 Ҁ1.80, 1.99 0.33 Ҁ1.22, 1.88 1.09 Ҁ0.04, 2.57 0.17 Ҁ1.31, 1.64 NS
Ratio of supine sagittal
abdominal diameter to
midthigh circumference
(҂100)
1.54
3
0.69, 2.39 1.28 Ҁ0.35, 2.91 0.90 Ҁ0.44, 2.23 0.33 Ҁ0.94, 1.61 2.09 0.82, 3.36 쏝0.01
Ratio of waist to midthigh
circumferences (҂ 100)
3.34
5
0.38, 6.29 1.84 Ҁ3.82, 7.50 1.79 Ҁ2.85, 6.44 2.28 Ҁ2.16, 6.72 2.71 Ҁ1.70, 7.13 NS
1
Values represent differences from control group (n ҃ 339). Estimates were obtained by linear regression and were adjusted for age, height, and clustering
of siblings. Estimates for specific 10-wk periods of gestational exposure were also adjusted for exposure in overlapping 10-wk periods. Estimates for any
exposure may reflect the additive effects of exposure in specific periods.
2
Values reflect the overall test of association of all 4 periods of exposure considered as a group (Wald test, 4 df).
3
P 쏝 0.01.
4
P 쏝 0.10.
5
P 쏝 0.05.
TABLE 6
Association of exposure to the Dutch famine overall or in the specified period of gestation with selected skinfold thicknesses in adulthood for persons
measured between 2003 and 2005
1
Period of gestational exposure
P
2
Overall Weeks 1–10 Weeks 11–20 Weeks 21–30
Week 31 to
delivery
Odds
ratio 95% CI
Odds
ratio 95% CI
Odds
ratio 95% CI
Odds
ratio 95% CI
Odds
ratio 95% CI
Subscapular
(n ҃ 929)
3
1.38
4
0.95, 1.99 0.87 0.43, 1.76 1.35 0.77, 2.37 1.09 0.64, 1.88 1.42 0.82, 2.44 NS
Tricipital (n ҃ 935)
3
1.30 0.89, 1.89 1.50 0.75, 3.00 1.16 0.64, 2.07 1.09 0.63, 1.91 1.37 0.79, 2.38 NS
Anterior midthigh
(n ҃ 760)
3
1.21 0.80, 1.81 1.18 0.57, 2.47 1.10 0.59, 2.06 1.35 0.73, 2.52 0.84 0.45, 1.58 NS
Ratio of subscapular to
tricipital (n ҃ 916)
5
1.55
6
1.08, 2.22 1.07 0.55, 2.08 1.67 0.96, 2.92 1.46 0.86, 2.49 1.09 0.63, 1.87 쏝0.10
1
Estimates were obtained by logistic regression and were adjusted for sex, age, height, and clustering of siblings. Tests for interaction by sex were not
significant (P 쏜 0.10). Estimates for specific 10-wk periods of gestational exposure were also adjusted for exposure in overlapping 10-wk periods.
2
Values reflect the overall test of association of all 4 periods of exposure considered as a group (Wald test, 4 df).
3
Odds ratios are for the highest quartile compared with all others.
4
P 쏝 0.10.
5
Odds ratios are for the group in which the subscapular skinfold is in a higher quartile than is the tricipital skinfold compared with all others.
6
P 쏝 0.05.
ANTHROPOMETRIC MEASURES AFTER MATERNAL UNDERNUTRITION 875
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participate in our study than were heavy women with no famine
exposure. We have no method to test for this potential bias,
however. We note that participation rates did not differ by sex or
by distance from the examination site. It is also possible that
parental characteristics associated with offspring adiposity dif-
fered by period of maternal exposure to famine. The effect of
such bias was minimized in our study because we selected con-
trol subjects from among siblings born outside of the famine
period (thus controlling for genetic sources of variation in adult
adiposity) and among births in the same institutions (thus minimiz-
ing social class differences between exposed and unexposed per-
sons). Adjustment for several variables that are themselves predic-
tors of adiposity, including measures of energy balance and, in
women, parity, did not affect our measures of association between
famine exposure and body mass distribution of the offspring.
In conclusion, exposure to the Dutch famine was strongly asso-
ciated with a wide range of indexes of body mass distribution in
middle-age women, and it was not associated with these indexes in
men or with measures of length or body proportions in either men or
women. These data suggest sex-specific, long-lasting effects of ma-
ternal undernutrition during pregnancy.
We thank the Vroedvrouwenscholen of Amsterdam and Rotterdam and
the Obstetrics Department of the Leiden University Medical Center for their
help in accessing their archives. The clinical examinations were carried out
at the study center of Gerontology & Geriatrics, Leiden University Medical
Center, under supervision of L de Man (head of study center).
LHL, ADS, and HSK developed the study hypothesis and study protocols,
designed the study, and developed and coordinated all data collection activ-
ities. LHL obtained the major funding. ADS conducted the data analysis and
wrote the initial drafts of the manuscript. LHL and HSK participated in the
data interpretation. KvdP participated in the development of the data collec-
tion protocols and initial data management and in data interpretation. PAZ
managed the files and data cleaning and participated in the data interpreta-
tion. AR participated in the data analysis and interpretation. All authors
reviewed and approved the final version of the manuscript. None of the
authors declared any financial conflict of interest.
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