European Journal of Clinical Nutrition (2004) 58, 894–900
& 2004 Nature Publishing Group All rights reserved 0954-3007/04 $30.00
www.nature.com/ejcn
ORIGINAL COMMUNICATION
Fetal growth is directly related to maternal
anthropometry and placental volume
M Thame1, C Osmond2, F Bennett1, R Wilks3 and T Forrester1*
1
Tropical Metabolism Research Unit, Tropical Medicine Research Institute, University of the West Indies, Mona, Kingston, Jamaica;
Medical Research Council Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital,
Southampton, UK; and 3Epidemiology Research Unit, Tropical Medicine Research Institute, University of the West Indies, Mona,
Kingston, Jamaica
2
Objective: To describe the influence of maternal weight and weight gain, placental volume and the rate of placental growth in
early pregnancy on fetal dimensions measured sonographically.
Design: In a prospective study, 712 women were recruited from the antenatal clinic of the University Hospital of the West Indies.
Data analysis was confined to 374 women on whom measurements of the placental volume at 14, 17 and 20 weeks gestation
were complete. Measurements of maternal anthropometry and fetal size (by ultrasound) were performed. Weight gain in
pregnancy between the first antenatal visit (8–10 weeks) and 20 weeks gestation, and the rate of growth of the placenta
between 14–17 and 17–20 weeks gestation were calculated.
Main outcome measures: Fetal anthropometry (abdominal and head circumferences, femoral length, and biparietal diameter)
at 35 weeks gestation.
Results: Lower maternal weight at the first antenatal visit was associated with a significantly smaller placental volume at 17 and
20 weeks gestation (Po0.002 and o0.0001 respectively). In all women, maternal weight gain was directly related to fetal
anthropometry. Placental volume at 14 weeks gestation and the rate of growth of the placenta between 17 and 20 weeks
gestation were significantly related to all four fetal measurements.
Conclusion: This study has provided evidence that both placental volume, and the rate of placental growth may influence fetal
size. These effects are evident in the first half of pregnancy, and appear to be mediated through maternal weight and weight
gain.
Sponsorship: This study was supported by a grant from the Wellcome Trust, 183 Euston Road, London, England.
European Journal of Clinical Nutrition (2004) 58, 894–900. doi:10.1038/sj.ejcn.1601909
Keywords: maternal weight; maternal weight gain; fetal anthropometry; placental volume
Introduction
*Correspondence: T Forrester, Tropical Metabolism Research Unit,
Tropical Medicine Research Institute, The University of the West Indies,
Mona, Kingston 7, Jamaica.
E-mail: terrence.forrester@uwimona.edu.jm
Contributors: All authors have read and approved submission of the
manuscript, and each has made a unique contribution to the study.
MT carried out the measurements on the subjects, supervised the
technical staff and participated in the writing and analysis of the
manuscript. CO provided statistical advice and participated in data
analysis. RW participated in the design of the study and was the
clinical epidemiologist assigned to conduct the study. FB participated
in the design of the study and the preparation of the manuscript. TF
was the principal investigator in all matters of the conduct of the
study, including the manuscript preparation. The project was
supported by the Wellcome Trust.
Received 25 September 2002; revised 6 March 2003; accepted 9 April
2003
Maternal anthropometry and other nutritional characteristics are known to influence birth weight (Kramer, 1987;
Thame et al, 1997), and in turn, weight at birth is related to
neonatal outcome and perinatal mortality (McCormick,
1985). Birth weight and newborn anthropometric proportions have long been of interest to public health researchers
and clinicians. The growing body of literature that has linked
size and proportions of the newborn with the risk of
developing coronary heart disease (Elford et al, 1991; Barker,
1997; Leon et al, 1998), hypertension (Barker et al, 1992;
Launer et al, 1993; Law & Sheill, 1996; Koupilova et al, 1999)
and diabetes mellitus (Barker et al, 1993; Lithell et al, 1996;
Rich-Edwards et al, 1999), has underlined the importance of
optimal fetal growth for health in later life.
Fetal growth and maternal anthropometry
M Thame et al
895
Maternal characteristics that influence birth weight include pre-pregnancy weight or maternal body mass index,
weight gain in pregnancy and maternal height, which are all
indicators of maternal nutritional status (Abrams & Selvin,
1995; World Health Organization, 1995; Kirchengast &
Hartmann, 1998). Genetic (Baker et al, 1993; Lui et al,
1993; Woods et al, 1996), environmental (Ericson et al, 1989;
England et al, 2001) and socioeconomic factors (Tuntiseranee
et al, 1999; Andersson et al, 2000) also influence birth weight,
as well as illnesses encountered in pregnancy such as
infections, hypertensive disorders and diabetes mellitus
(Ananth et al, 1995; Lauszus et al, 1999).
The growth of the fetus during intrauterine life is reflected
in the weight at birth. Fetal growth is largely determined by
the availability of nutrients from the mother, as well as
placental capacity to supply these nutrients in sufficient
quantities to the fetus (Hay, 1991; Paneth & Susser, 1995).
Maternal weight may be a marker of macronutrient availability, and through the flow of nutrients to the fetoplacental unit, can theoretically exert an influence on fetal growth
(Gluckman et al, 1990).
Placental transport, metabolic and endocrine functions
are major determinants of fetal nutrition and homeostasis
(Hay, 1991; Anthony et al, 1995), and placental capacity is
crudely related to the weight of the organ. Traditionally,
placental weight is measured at birth and the relationship
of placental weight to birth weight has been used to
indicate adequacy of fetal nutrition. However, there is
limited information on the relationship between intrauterine placental volume and birth weight (Wolf et al, 1989;
Clapp et al, 1995; Kinare et al, 2000; Thame et al, 2001).
Although placental weight at delivery may be an important
determinant of birth weight, both the pattern and rate
of growth of the placenta throughout pregnancy are
expected to be important contributors. There is an extensive
literature describing the effect of maternal anthropometry
on birth weight, but there is a paucity of information
describing the relationships between and among maternal
anthropometry, placental volume in early pregnancy, and
fetal size. The aim of this study was to describe the
relationships between maternal weight and weight gain,
placental volume and the rate of placental growth in
early pregnancy and sonographic measurements of fetal
dimensions.
Methods
A total of 712 women making their first visit to the antenatal
clinic at the University Hospital of the West Indies, Kingston,
Jamaica, were invited to participate in a prospective study
investigating maternal determinants of fetal growth. Recruitment was restricted to women who were aged between 15
and 40 y, were 7–10 weeks pregnant, sure of their last
menstrual period, and without systemic illnesses such as
pre-eclampsia and diabetes, or genetic abnormality, for
example, sickle cell disease. Of the 712 women recruited,
569 completed the study. The other 143 were lost to the
study for a variety of reasons. In all, 82 experienced
pregnancy losses, 56 withdrew for reasons such as work
constraints, migration or fear that ultrasonography would
harm their fetus, and there were five sets of twins. All women
were offered transportation to and from the hospital to
enhance participation in the study. For this report, data
analysis was confined to the 374 women on whom
measurements of placental volume at 14, 17 and 20 weeks
gestation were complete.
Three individuals, MT, a nurse and a medical technologist,
made all measurements. Two of the three observers made the
ultrasound measurements (MT and the technologist). All
three were trained to apply the questionnaires and make the
measurements. At the start, and at three monthly intervals
for the duration of the study, inter- and intraobserver
measurement variability were assessed, and training and
recertification prescribed for any observer whose scores were
not acceptable (Thame et al, 2000). Inter- and intraobserver
variability for ultrasound measurements had a correlation
coefficient greater than 0.99 throughout the study. Smoking,
alcohol and drug use were determined from questionnaire
responses, and a rating scale, based on social amenities and
possessions was used to define socioeconomic status (Forrester et al, 1996; Thame et al, 2000). The Ethics Committee
of the Faculty of Medical Sciences, The University of the
West Indies approved the study.
At each visit, maternal weight was measured to the nearest
0.01 kg using a Weylux beam balance (CMS Weighing
Equipment Ltd, London, UK), height to the nearest 0.1 cm
using a stadiometer (CMS Weighing Equipment Ltd, London, UK) and blood pressure with an oscillometric sphygmomanometer (Dinamap TM monitor Model 8100, Critikon
Inc.). Hemoglobin was measured with a Coulter counter
(Coulter Electronics, Inc.) at the first visit.
Sonographic measurements (linear probe, ATL Ultramark
IV; Advanced Technology Labs, Bothell, WA, USA) of fetus
and placenta were made at 14, 17, 20, 25, 30 and 35 weeks of
gestation to determine the changes in size with gestational
age. The method used to measure placental volume required
that the entire placenta be seen on the screen. After 20 weeks
gestation, many placentas are too large for this, so placental
volume was measured at only the first three visits; fetal
biparietal diameter, femoral length, and head and abdominal
circumferences were measured at all six visits. The average of
three repeats was used for each measurement. Placental
volume was measured by identifying and recording on
videotape, the long axis of the placenta. A continuous
recording of the image of the placenta orthogonal to the axis
was made by sweeping the probe along the axis at constant
velocity. This axis was divided into six sections of equal
length; the five interior cross-sectional areas were measured
and integrated to estimate the placental volume. This
method was developed and validated by Howe et al (1994).
Multiple linear regression and comparison of means were
used to analyze the data. Placental volumes were rightEuropean Journal of Clinical Nutrition
Fetal growth and maternal anthropometry
M Thame et al
896
skewed, and thus, were square-root transformed to normality. They were then adjusted for gestational age. Weight gain
in early pregnancy between the first antenatal visit (8–10
weeks) and 20 weeks gestation, the rate of growth of the
placenta between 14 and 17 weeks and 17 and 20 weeks
gestation were calculated. Maternal weight at the first
antenatal visit, weight gain in early pregnancy, gender and
gestational age were the main independent variables used in
regression analyses. In the regression models, fetal measurements (abdominal circumference, femoral length, head
circumference and biparietal diameter) at 35 weeks gestation
were the dependent variables. The hypotheses being tested
were that maternal weight at the first antenatal visit, weight
gain, placental volume and the rate of placental growth in
early pregnancy are related to sonographic measurements of
fetal dimensions.
Results
Mean maternal measurements of the study group at 6376
days gestation are given in Table 1. The 338 women who
Table 1 Maternal and newborn characteristics
Variables
Mean
First Antenatal Visit
Weight (kg)
Height (cm)
Body mass index (kg/m2)
Hemoglobin (g/dl)
Systolic blood pressure (mmHg)
Diastolic blood pressure (mmHg)
Gestational age (days)
65.5
163.5
24.5
12.2
109.5
63.0
63.0
s.d.
Range
n
13.1 32.9–114.4
163.5 144.5–182.8
4.6 14.8–37.9
1.1
8.8–15.5
9.8 87.3–140.7
7.9 40.7–84.7
6.0
46–84
374
374
374
360
369
369
374
Newborn
Birth weight (kg)
3.13
0.6
0.5–4.7
355
Head circumference (cm)
34.3
1.7 27.3–44.5
345
Crown–heel length (cm)
49.4
2.9 39.2–55.6
343
Mid-upper-arm circumference (cm) 10.3
1.0
5.3–13.5
339
Abdominal circumference (cm)
30.7
2.4 21.5–37.5
339
Chest circumference (cm)
32.4
2.2 23.5–41.5
341
Placental weight (g)
571.1 136.1 142.0–1200.0 349
Gestational age (days)
275.0
14.0 197–299
355
failed to complete the study were no different in age or
anthropometry from the 374 women who did form the basis
of this report (data not shown). Hemoglobin concentration
was not available for 14 women, and blood pressure
measurements were not successfully made in five patients.
There was also no difference in newborn anthropometry
between the two groups (data not shown). Mean neonatal
measurements are shown in Table 1. Ten women in the study
had pregnancy losses and nine women migrated, accounting
for the difference between the number of maternal measurements and birth weight seen in Table 1. As expected, fetal
and placental measurements gradually increased throughout
pregnancy (Table 2). Also, it appears that ultrasound
measurements are a reasonable index of fetal growth
compared to measurements made at birth. Correspondingly,
abdominal circumference at 35 weeks is highly positively
correlated with birth weight (r¼0.62, Po0.001), and placental volume measured at 20 weeks is highly positively
correlated with placental weight (r¼0.46, Po0.001).
In order to explore the relationships between maternal
weight and placental volume, the women were stratified into
groups of maternal weight, beginning at r55 kg and
increasing by 10 kg, based on maternal weight at the first
antenatal visit. Those with lower maternal weight had a
significantly smaller placental volume at 17 and 20 weeks
gestation (Po0.002 and o0.0001, respectively) compared to
women with higher maternal weight (Table 3 and Figure 1).
Similarly, there was a direct relationship between maternal
body mass index and placental volume at 14, 17 and 20
weeks gestation. Hence, a 1 kg/m2 increment in mother’s
body mass index (BMI) at booking is associated with a 0.08
(95% CI¼0.01–0.14)-unit increase in the square root of
placental volume at 14 weeks gestation (P¼0.02); with a 0.07
(95% CI¼0.01–0.13)-unit increase at 17 weeks (P¼0.026);
and with a 0.1 (95% CI¼0.04–0.16)-unit increase at 20 weeks
(P¼0.001).
The simultaneous contributions of maternal weight and
weight gain to fetal growth were also explored. Both
maternal weight and maternal weight gain were stratified
into groups, and were directly related to fetal abdominal
circumference at 35 weeks. In any category of maternal
Table 2 Fetoplacental measurements from 14 to 35 weeks gestation
Gestation (weeks)
14
Variable
BPD (mm)
HC (mm)
AC (mm)
FL (mm)
PV (ml)
Mean
28.8
98.5
85.9
15.0
116.5
(371)
(371)
(366)
(369)
(374)
17
s.d.
3.2
12.2
11.4
3
52.3
Mean
38.9
137.2
120.0
24.6
242.9
(373)
(372)
(372)
(372)
(374)
20
s.d.
3.3
11.8
11.1
3.1
73.4
Mean
48.6
173.6
152.6
33.6
359.8
(372)
(373)
(373)
(372)
(374)
25
s.d.
3.3
12.1
11.9
2.9
84.5
Mean
64.1
229.7
206.9
46.7
(321)
(321)
(322)
(322)
30
s.d.
3.6
12.4
14.4
3.1
Mean
77.7
276.9
262.8
58.4
(318)
(318)
(318)
(318)
35
s.d.
3.6
12.4
16.8
3
Mean
87.2
309.4
314.6
68.9
(309)
(309)
(309)
(308)
s.d.
3.4
11.7
18.6
3.2
Number of subjects within the brackets. BPD¼biparietal diameter; HC¼head circumference; AC¼abdominal circumference; FL¼femoral length; PV¼placental
volume.
European Journal of Clinical Nutrition
Fetal growth and maternal anthropometry
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897
Table 3 Effect of maternal weight at the first antenatal visit on placental volume at 14, 17 and 20 weeks gestation
Placental Volume (ml)
Weight (kg)
14 week
s.d.
17 week
s.d.
20 week
s.d.
n
r55
55.1–65.0
65.1–75.0
475.1
Total
P
118
110.2
115.9
124.4
116.5
0.17
46.9
52.3
54.1
54.7
52.3
227.6
236.9
247.7
259.9
242.9
0.002
70.7
72
76.2
71.9
73.4
330.7
353.5
374
380
359.8
0.0001
80.9
83.4
94.3
70.4
84.5
79
118
89
88
374
was used in the regression analysis. Both gender and
gestational age are known to have an effect on fetal growth,
hence, these were controlled for in the regression model.
Table 5 shows the effects of maternal weight, weight gain,
placental volume and rate of placental growth on fetal
measurements (biparietal diameter, femoral length, abdominal and head circumference). Placental volume at 14 weeks
gestation and the rate of growth of the placenta between 17
and 20 weeks gestation were significantly related to all four
fetal measurements. In further analyses when placental
volume at 20 weeks gestation was added to the model, the
14-week placental volume still independently contributed to
fetal growth at 35 weeks gestation (data not shown). The rate
of growth of the placenta between 14 and 17 weeks gestation
was significantly associated with fetal abdominal circumference and the femoral length at 35 weeks gestation.
Abdominal circumference was the only fetal measurement
that was significantly associated with maternal weight at the
first antenatal visit. Weight gain early in pregnancy was
associated with all fetal measurements except femoral length.
The fetal measurements made were not associated with
maternal socioeconomic status. Less than 1% of mothers
reported the use of alcohol or tobacco, and none admitted to
the use of illegal drugs.
Figure 1 Lines were drawn using the mean values of early weight
gain between the respective dates of measurement; sex of child is
female; parity is in the third quartile.
weight, maternal weight gain was directly related to fetal
abdominal circumference (Table 4). Thus, women whose
fetuses had the largest abdominal circumference were those
who were heaviest at the first antenatal visit and gained the
greatest amount of weight in early pregnancy (Table 4). This
analysis was repeated for the other three fetal measurements,
biparietal diameter, head circumference and femoral length,
and similar results were obtained (data not shown). Placental
volumes at 14, 17 and 20 weeks gestation were highly
correlated, therefore, the earliest measurement (14 weeks)
Discussion
This study reports on the inter-relationship of first trimester
maternal weight, subsequent weight gain in pregnancy,
Table 4 Maternal weight at the first antenatal visit and early weight gain on fetal abdominal circumference at 35 weeks gestation
Abdominal circumference (mm)
Maternal weight (kg) at the first antenatal visit
Weight gain (kg/4 weeks)
r55
55.1–65.0
65.1–75.0
475.1
Total
r0.5
0.51–1.00
1.00–1.50
41.50
297.8(6)
299.4(14)
313.7(20)
310.4(24)
309.5(18)
316.1(20)
315.8(25)
318.0(31)
302.3(23)
314.4(13)
310.6(16)
326.3(24)
317.5(26)
315.5(16)
318.2(10)
327.5(23)
309.1(73)
311.9(63)
314.4(71)
320.3(102)
Total
307.8(64)
315.4(94)
313.7(76)
320.2(75)
314.6(309)
Subscripts give number of subjects. P-value for trend o0.001 for maternal weight (kg) at the first antenatal visit on fetal abdominal circumference at 35 weeks
gestation. [2] P-value for trend o0.001 for early weight gain (kg/4 weeks) on fetal abdominal circumference at 35 weeks gestation.
European Journal of Clinical Nutrition
Fetal growth and maternal anthropometry
M Thame et al
898
Table 5 Maternal weight at the first antenatal visit, early weight gain, placental volume, rate of placental growth and fetal measurements at 35 weeks
gestation: multiple regression analysis
Outcome variables are fetal measurements at 35 weeks gestation (mm)
Abdominal circumference
Variable
Gender (male¼1, female¼2)
Gestational age at 35 weeks gestation (days)
Placental volume at 14 weeks (s.d.)(ml)
Rate of placental growth between 14 and
17 weeks gestation (ml/day)
Rate of placental growth between 17 and
20 weeks gestation (ml/day)
Maternal weight (kg) at the first antenatal visit
Early maternal weight gain (first antenatal
visit20 weeks gestation) (kg/4 weeks)
Constant
Adjusted R2
Femoral length
Head circumference
Biparietal diameter
B
SEB
B
SEB
B
SEB
B
SEB
2.09
1.11
8.34
102.80
1.77
0.16z
1.15z
22.65z
0.08
0.23
1.09
11.82
0.32
0.03z
0.21z
4.10w
4.14
0.43
3.33
27.69
1.26w
0.11z
0.82z
16.17
0.83
0.18
1.10
7.56
0.35*
0.03z
0.23z
4.44
98.35
21.79z
14.58
3.95z
36.52
15.56*
13.52
4.28w
0.19
4.35
0.07w
0.99z
0.01
0.19
0.01
0.18
0.04
1.61
0.05
0.70*
0.02
0.52
0.01
0.19w
10.55
25.0
7.03
204.51
14.9
43.76
21.2
7.66
27.8
33.4
39.00
27.84
B is the regression coefficient. *Po0.05; wPo0.01; zPo0.001.
placental volumes in early pregnancy and fetal
growth. In previous reports, birth weight and anthropometry at birth have been the outcome variables
measured and a positive relationship between maternal
weight and birth weight has been reported (Kramer 1987;
Thame et al, 1997; Kirchengast & Hartmann, 1998). In
the present study, maternal first trimester weight and
weight gain in pregnancy were directly related to indices of
fetal growth.
In assessing fetal size, it is customary that four fetal
measurements are considered, biparietal diameter, femoral
length, head and abdominal circumferences. The measurements at 35 weeks gestation were chosen as the outcome
variables, as in previous analyses (data not shown), associations of maternal weight and fetal measurements were not
seen until the 25th week of gestation. In assessing the
relationships of placental volume and maternal weight gain
in early pregnancy with fetal measurements, the last
recorded fetal measurement, which was at 35 weeks gestation, was used.
Low maternal weight in the first trimester, a proxy
measure of poor nutritional status, was associated with a
smaller placenta and a smaller fetal abdominal circumference at 35 weeks gestation. Maternal weight gain in early
pregnancy proved to be a more important predictor of fetal
size than maternal weight at the first antenatal visit. All fetal
measurements except femoral length showed a significant
positive association with weight gain early in pregnancy and
women who had a lower rate of weight gain delivered
smaller babies than mothers who had a higher rate of weight
gain. In previous studies, weight gain in pregnancy has also
been shown to be an important contributor to birth weight
(Abrams & Selvin, 1995). It is possible that this influence on
fetal size could be exerted through the adequacy of
European Journal of Clinical Nutrition
placentation and indeed, lighter mothers had a smaller
placental volume at every stage of pregnancy.
The placenta is established early in intrauterine life, and its
rapid growth in the early part of pregnancy is important for
the supply of the nutrients necessary to ensure adequate fetal
growth. The placenta exerts its effects on the growth of the
fetus from the beginning of pregnancy by way of its
transport, metabolic and endocrine functions (Anthony
et al, 1995). The growth trajectory of the placenta is
influenced by maternal size and nutrition before and during
early pregnancy and the rate of growth of the organ is
initially greater than that of the rate of growth of the fetus
(Hendricks, 1964), in order to prepare the supply line
necessary for fetal growth.
This study also examined the effects of placental volume
in early pregnancy, and the relationship between the rate of
placental growth between 14–17 and 17–20 weeks gestation
and fetal size. Although other studies have examined the
effect of placental volume on birth weight (Wolf et al, 1989;
Clapp et al, 1995; Thame et al, 2001), this study contributes
important information on the effect of placental volume as
well as the rate of placental growth in early pregnancy on
fetal size (Clapp et al, 2000, 2002). Placental volume at 14
weeks gestation showed a significant positive association
with all fetal measurements. Although the rate of growth of
the placenta between 14 and 17 weeks gestation was an
important determinant of abdominal circumference and
femoral length, it was the rate of growth of the placenta
between 17 and 20 weeks gestation that showed significant
positive associations with all of the fetal measurements. This
may imply that this period of gestation is important in
determining fetal size.
Smaller babies at birth are thought to be at increased risk
for chronic disease in adult life (Barker, 1997; Leon et al,
Fetal growth and maternal anthropometry
M Thame et al
899
1998), and this study has shown that maternal nutrition, as
measured by maternal weight and the rate of maternal
weight gain in pregnancy, influences fetal size and hence
birth weight (Thame et al, 2001). Placental volume and the
rate of placental growth are also influenced by maternal
weight, and in turn, also contribute to fetal size. One
implication of these results is that by securing catch up
weight in undernourished mothers, it may be possible to
improve fetal growth. Such a finding would hold important
public health implications.
In conclusion, this study has provided evidence of a
significant influence of both placental volume, and the rate
of placental growth, in determining fetal size and ultimately,
birth weight. These effects appear to be mediated through
maternal weight and weight gain in pregnancy and suggest
that these events determining fetal size operate early in
pregnancy.
References
Abrams B & Selvin S (1995): Maternal weight gain pattern and birth
weight. Obstet. Gynecol. 86, 63–69.
Andersson SW, Niklasson A, Lapidus L, Hallberg L, Bengtsson C &
Hulthen L (2000): Sociodemographic characteristics influencing
birth outcome in Sweden, 1908–1930. Birth variables in the
population study of women in Guthenburg. J. Epidemiol. Community Health 54, 269–278.
Ananth CV, Peedicayil A & Savitz DA (1995): Effect of hypertensive disease in pregnancy on birthweight, gestational
duration and small-for-gestational age births. Epidemiology 6,
391–395.
Anthony RV, Pratt Sl, Liang R & Holland MD (1995): Placental–fetal
hormonal interactions: impact on fetal growth. J. Anim. Sci. 73,
1861–1871.
Baker J, Lui JP, Robertson EJ & Efstratiadis A (1993): Role of insulinlike growth factors in embryonic and postnatal growth. Cell 75,
73–82.
Barker DJP (1997): The fetal origins of coronary heart disease. Acta
Paediatr. 422(Suppl.), S78–S82.
Barker DJP, Godfrey KM, Osmond C & Bull A (1992): The relationship
of fetal length, ponderal index and head circumference to blood
pressure and risk of hypertension in adult life. Paediatr. Perinat.
Epidemiol. 6, 35–44.
Barker DJP, Hales CN, Fall CHD, Osmond C, Phipps K & Clark PMS
(1993): Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced
fetal growth. Diabetologia. 36, 62–67.
Clapp III JF, Rizk KH, Appleby-Wineberg SK & Crass JR (1995):
Second-trimester placental volumes predicts birth weight at term.
J. Soc. Gynecol. Invest. 2, 19–22.
Clapp III JF, Kim H, Burciu B & Lopez B (2000): Beginning regular
exercise in early pregnancy: effect on fetoplacental growth. Am. J.
Obstet. Gynecol. 183, 1484–1488.
Clapp III JF, Kim H, Burciu B, Schmidt S, Petry K & Lopez B (2002):
Continuing regular exercise during pregnancy: effect of exercise
volume on fetoplacental growth. Am. J. Obstet. Gynecol. 186,
142–147.
Elford J, Whincup P & Shaper AG (1991): Early life experiences and
cardiovascular disease: longitudinal and case–control studies. Int.
J. Epidemiol. 20, 833–844.
England LJ, Kendrick JS, Wilson HG, Merritt RK, Gargiullo PM &
Zahniser SC (2001): Effects of smoking reduction during pregnancy on the birth weight of term infants. Am. J. Epidemiol. 154,
694–701.
Ericson A, Eriksson M, Kallen B & Zetterstrom R (1989): Socioeconomic variables and pregnancy outcome. Birthweight in
singletons. Acta Paediatr. Scand. 360(Suppl.), S48–S55.
Forrester TE, Wilks RJ, Bennett FI, Simeon D, Osmond C,
Allen M, Chung AP & Scott P (1996): Fetal growth and
cardiovascular risk factors in Jamaican schoolchildren. BMJ 312,
156–160.
Gluckman PD, Breier BH, Oliver M, Harding J & Bassett N (1990):
Fetal growth in late gestation—a constrained pattern of growth.
Acta Paediatr. Scand. 367, 105–110.
Hay WW (1991): The placenta. Not just a conduit for maternal fuels.
Diabetes 40, 44–50.
Hendricks CH (1964): Patterns of fetal and placental growth:
the second half of normal pregnancy. Obstet. Gynecol. 24,
357–365.
Howe D, Wheeler & Perring S (1994): Measurement of placental
volume with real time ultrasound in mid-pregnancy. J. Clin.
Ultrasound 22, 77–83.
Kinare AS, Natekar AS, Chinchwadkar MC, Yajnik CS, Coyaji KJ, Fall
CH & Howe DT (2000): Low mid-pregnancy placental volume in
rural Indian women: a cause for low birth weight. Am. J. Obstet.
Gynecol. 182, 443–448.
Kirchengast S & Hartmann B (1998): Maternal prepregnancy
weight status and pregnancy weight gain as major determinants for newborn weight and size. Ann. Hum. Biol. 25,
17–28.
Koupilova I, Leon DA, McKeigue PM & Lithell HO (1999):
Is the effect of low birth weight on cardiovascular
mortality mediated through high blood pressure? J. Hypertens.
17, 19–25.
Kramer MS (1987): Determinants of low birth weight: methodological assessment and meta-analysis Bull. World Health Organ. 65,
663–737.
Launer LJ, Hofman A & Grobbee DE (1993): Relation between birth
weight and blood pressure: longitudinal study of infants and
children. BMJ 307, 1451–1454.
Lauszus FF, Paludan J & Klebe JG (1999): Birthweight in women
with potential gestational diabetes mellitus—an effect of obesity
rather than glucose intolerance? Acta Obstet. Gynecol. Scand. 78,
520–525.
Law CM & Sheill AW (1996): Is blood pressure inversely
related to birth weight? The strength of the evidence from
a systematic review of the literature. J. Hypertens. 14,
935–941.
Leon DA, Lithell HO, Vagero D, Koupilova I, Mohsen R & Berglund L
(1998): Reduced fetal growth rate and increased risk of death from
ischaemic heart disease: cohort study of 15000 Swedish men and
women born 1915–29. BMJ 317, 241–244.
Lithell HO, McKeigue PM, Berglund L, Mohsen R, Lithell UB & Leon
DA (1996): Relation of size at birth to non-insulin dependent
diabetes and insulin concentrations in men aged 50–60 years. BMJ
312, 406–410.
Lui JP, Baker J, Perkins AS, Robertson EJ & Efstratiadis A (1993):
Mice carrying null mutations of the genes encoding insulin-like
growth factor I (IGF-I) and type I IGF receptor (IGFIr). Cell 75,
59–72.
McCormick MC (1985): The contribution of low birth weight
to infant mortality and childhood morbidity. N. Engl. J. Med.
312, 82–90.
Paneth N & Susser M (1995): Early origin of coronary heart disease
(the ‘‘Barker hypothesis’’). BMJ 310, 411–412.
Rich-Edwards JW, Colditz GA, Stampfer MJ, Willett WC, Gillman
MW, Hennekens CH, Speizer FE & Manson JE (1999): Birthweight
and risk of type 2 diabetes mellitus in adult women. Ann. Intern.
Med. 130, 278–284.
Thame M, Wilks RJ, McFarlane-Anderson N, Bennett FI & Forrester
TE (1997): Relationship between maternal nutritional status and
infant’s weight and body proportions at birth. Eur. J. Clin. Nutr. 51,
134–138.
European Journal of Clinical Nutrition
Fetal growth and maternal anthropometry
M Thame et al
900
Thame M, Osmond C, Wilks RJ, Bennett FI, McFarlane-Anderson &
Forrester TE (2000): Blood pressure is related to placental volume
and birth weight. Hypertension 35, 662–667.
Thame M, Osmond C, Wilks RJ, Bennett FI & Forrester TE (2001):
Second trimester placental volume and infant size at birth. Obstet.
Gynecol. 98, 279–283.
Tuntiseranee P, Olsen J, Chongsuvivatwong V & Limbutara S (1999):
Socioeconomic and work related determinants of pregnancy
outcome in southern Thailand. J. Epidemiol. Community Health
53, 624–629.
European Journal of Clinical Nutrition
Wolf H, Oosting H & Treffers P (1989): Second-trimester placental
volume measurement by ultrasound: prediction of fetal outcome.
Am. J. Obstet. Gynecol. 160, 121–126.
Woods KA, Camacho Hubner C, Savage MO & Clark AJ (1996):
Intrauterine growth retardation and postnatal growth failure
associated with deletion of the insulin-like growth factor I gene.
N. Engl. J. Med. 335, 1363–1367.
World Health Organization (1995): Maternal anthropometry
and pregnancy outcome Bull. World Health Organ 73,
21–31.