European Journal of Clinical Nutrition (2004) 58, 894900

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ORIGINAL COMMUNICATION
Fetal growth is directly related to maternal anthropometry and placental volume
M Thame1, C Osmond2, F Bennett1, R Wilks3 and T Forrester1*
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 1

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 (810 weeks) and 20 weeks gestation, and the rate of growth of the placenta between 1417 and 1720 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, 894900. 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.

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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. 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

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 710 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,

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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 (810 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. 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 (r0.62, Po0.001), and placental volume measured at 20 weeks is highly positively correlated with placental weight (r0.46, 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 mothers body mass index (BMI) at booking is associated with a 0.08 (95% CI0.010.14)-unit increase in the square root of placental volume at 14 weeks gestation (P0.02); with a 0.07 (95% CI0.010.13)-unit increase at 17 weeks (P0.026); and with a 0.1 (95% CI0.040.16)-unit increase at 20 weeks (P0.001). 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

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 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) Mean s.d. Range n

65.5 163.5 24.5 12.2 109.5 63.0 63.0

13.1 32.9114.4 163.5 144.5182.8 4.6 14.837.9 1.1 8.815.5 9.8 87.3140.7 7.9 40.784.7 6.0 4684

374 374 374 360 369 369 374

Newborn Birth weight (kg) 3.13 0.6 0.54.7 355 Head circumference (cm) 34.3 1.7 27.344.5 345 Crownheel length (cm) 49.4 2.9 39.255.6 343 Mid-upper-arm circumference (cm) 10.3 1.0 5.313.5 339 Abdominal circumference (cm) 30.7 2.4 21.537.5 339 Chest circumference (cm) 32.4 2.2 23.541.5 341 Placental weight (g) 571.1 136.1 142.01200.0 349 Gestational age (days) 275.0 14.0 197299 355

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) s.d. 3.2 12.2 11.4 3 52.3 17 Mean 38.9 137.2 120.0 24.6 242.9 (373) (372) (372) (372) (374) s.d. 3.3 11.8 11.1 3.1 73.4 20 Mean 48.6 173.6 152.6 33.6 359.8 (372) (373) (373) (372) (374) s.d. 3.3 12.1 11.9 2.9 84.5 25 Mean 64.1 229.7 206.9 46.7 (321) (321) (322) (322) s.d. 3.6 12.4 14.4 3.1 30 Mean 77.7 276.9 262.8 58.4 (318) (318) (318) (318) s.d. 3.6 12.4 16.8 3 35 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. BPDbiparietal diameter; HChead circumference; ACabdominal circumference; FLfemoral length; PVplacental volume.

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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) r55 55.165.0 65.175.0 475.1 Total P 14 week 118 110.2 115.9 124.4 116.5 0.17 s.d. 46.9 52.3 54.1 54.7 52.3 17 week 227.6 236.9 247.7 259.9 242.9 0.002 s.d. 70.7 72 76.2 71.9 73.4 20 week 330.7 353.5 374 380 359.8 0.0001 s.d. 80.9 83.4 94.3 70.4 84.5 n 79 118 89 88 374

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)

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.

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) r0.5 0.511.00 1.001.50 41.50 Total r55 297.8(6) 299.4(14) 313.7(20) 310.4(24) 307.8(64) 55.165.0 309.5(18) 316.1(20) 315.8(25) 318.0(31) 315.4(94) 65.175.0 302.3(23) 314.4(13) 310.6(16) 326.3(24) 313.7(76) 475.1 317.5(26) 315.5(16) 318.2(10) 327.5(23) 320.2(75) Total 309.1(73) 311.9(63) 314.4(71) 320.3(102) 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.

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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 (male1, female2) 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 B 2.09 1.11 8.34 102.80 98.35 0.19 4.35 27.8 33.4 SEB 1.77 0.16z 1.15z 22.65z 21.79z 0.07w 0.99z 39.00 Femoral length B 0.08 0.23 1.09 11.82 14.58 0.01 0.19 10.55 25.0 SEB 0.32 0.03z 0.21z 4.10w 3.95z 0.01 0.18 7.03 Head circumference B 4.14 0.43 3.33 27.69 36.52 0.04 1.61 204.51 14.9 SEB 1.26w 0.11z 0.82z 16.17 15.56* 0.05 0.70* 27.84 Biparietal diameter B 0.83 0.18 1.10 7.56 13.52 0.02 0.52 43.76 21.2 SEB 0.35* 0.03z 0.23z 4.44 4.28w 0.01 0.19w 7.66

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 1417 and 1720 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,

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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.
Ericson A, Eriksson M, Kallen B & Zetterstrom R (1989): Socioeconomic variables and pregnancy outcome. Birthweight in singletons. Acta Paediatr. Scand. 360(Suppl.), S48S55. 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, 156160. Gluckman PD, Breier BH, Oliver M, Harding J & Bassett N (1990): Fetal growth in late gestationa constrained pattern of growth. Acta Paediatr. Scand. 367, 105110. Hay WW (1991): The placenta. Not just a conduit for maternal fuels. Diabetes 40, 4450. Hendricks CH (1964): Patterns of fetal and placental growth: the second half of normal pregnancy. Obstet. Gynecol. 24, 357365. Howe D, Wheeler & Perring S (1994): Measurement of placental volume with real time ultrasound in mid-pregnancy. J. Clin. Ultrasound 22, 7783. 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, 443448. 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, 1728. 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, 1925. Kramer MS (1987): Determinants of low birth weight: methodological assessment and meta-analysis Bull. World Health Organ. 65, 663737. Launer LJ, Hofman A & Grobbee DE (1993): Relation between birth weight and blood pressure: longitudinal study of infants and children. BMJ 307, 14511454. Lauszus FF, Paludan J & Klebe JG (1999): Birthweight in women with potential gestational diabetes mellitusan effect of obesity rather than glucose intolerance? Acta Obstet. Gynecol. Scand. 78, 520525. 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, 935941. 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 191529. BMJ 317, 241244. 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 5060 years. BMJ 312, 406410. 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, 5972. McCormick MC (1985): The contribution of low birth weight to infant mortality and childhood morbidity. N. Engl. J. Med. 312, 8290. Paneth N & Susser M (1995): Early origin of coronary heart disease (the Barker hypothesis). BMJ 310, 411412. 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, 278284. Thame M, Wilks RJ, McFarlane-Anderson N, Bennett FI & Forrester TE (1997): Relationship between maternal nutritional status and infants weight and body proportions at birth. Eur. J. Clin. Nutr. 51, 134138.

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