Maternal Nut

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ORIGINAL COMMUNICATION

Fetal growth is directly related to maternalanthropometry and placental volumeM Thame 1 , C Osmond 2 , F Bennett 1 , R Wilks 3 and T Forrester 1 *

1 Tropical Metabolism Research Unit, Tropical Medicine Research Institute, University of the West Indies, Mona, Kingston, Jamaica;2 Medical Research Council Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital,Southampton, UK; and 3 Epidemiology Research Unit, Tropical Medicine Research Institute, University of the West Indies, Mona, Kingston, Jamaica

Objective: To describe the influence of maternal weight and weight gain, placental volume and the rate of placental growth inearly 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 gestationwere complete. Measurements of maternal anthropometry and fetal size (by ultrasound) were performed. Weight gain inpregnancy between the first antenatal visit (810 weeks) and 20 weeks gestation, and the rate of growth of the placentabetween 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 and20 weeks gestation ( P o 0.002 and o 0.0001 respectively). In all women, maternal weight gain was directly related to fetalanthropometry. Placental volume at 14 weeks gestation and the rate of growth of the placenta between 17 and 20 weeksgestation 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 fetalsize. These effects are evident in the first half of pregnancy, and appear to be mediated through maternal weight and weightgain.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

IntroductionMaternal anthropometry and other nutritional characteris-tics 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 propor-tions have long been of interest to public health researchersand clinicians. The growing body of literature that has linkedsize 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.

Received 25 September 2002; revised 6 March 2003; accepted 9 April2003

*Correspondence: T Forrester, Tropical Metabolism Research Unit,Tropical Medicine Research Institute, The University of the West Indies,Mona, Kingston 7, Jamaica.E-mail: [email protected] : All authors have read and approved submission of themanuscript, and each has made a unique contribution to the study.MT carried out the measurements on the subjects, supervised thetechnical staff and participated in the writing and analysis of themanuscript. CO provided statistical advice and participated in dataanalysis. RW participated in the design of the study and was theclinical epidemiologist assigned to conduct the study. FB participatedin the design of the study and the preparation of the manuscript. TFwas the principal investigator in all matters of the conduct of thestudy, including the manuscript preparation. The project wassupported by the Wellcome Trust.

European Journal of Clinical Nutrition (2004) 58,894900& 2004 Nature Publishing Group All rights reserved 0954-3007/04 $30.00

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Maternal characteristics that influence birth weight in-clude pre-pregnancy weight or maternal body mass index,weight gain in pregnancy and maternal height, which are allindicators 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 (Tuntiseraneeet al , 1999; Andersson et al , 2000) also influence birth weight,as well as illnesses encountered in pregnancy such asinfections, hypertensive disorders and diabetes mellitus(Ananth et al , 1995; Lauszus et al , 1999).

The growth of the fetus during intrauterine life is reflectedin the weight at birth. Fetal growth is largely determined bythe availability of nutrients from the mother, as well asplacental capacity to supply these nutrients in sufficientquantities to the fetus (Hay, 1991; Paneth & Susser, 1995).Maternal weight may be a marker of macronutrient avail-ability, and through the flow of nutrients to the fetoplacen-tal unit, can theoretically exert an influence on fetal growth(Gluckman et al , 1990).

Placental transport, metabolic and endocrine functionsare major determinants of fetal nutrition and homeostasis(Hay, 1991; Anthony et al , 1995), and placental capacity iscrudely related to the weight of the organ. Traditionally,placental weight is measured at birth and the relationshipof placental weight to birth weight has been used toindicate adequacy of fetal nutrition. However, there islimited information on the relationship between intrauter-ine 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 rateof growth of the placenta throughout pregnancy areexpected to be important contributors. There is an extensiveliterature describing the effect of maternal anthropometryon birth weight, but there is a paucity of informationdescribing the relationships between and among maternalanthropometry, placental volume in early pregnancy, andfetal size. The aim of this study was to describe therelationships between maternal weight and weight gain,placental volume and the rate of placental growth inearly pregnancy and sonographic measurements of fetaldimensions.

MethodsA total of 712 women making their first visit to the antenatalclinic at the University Hospital of the West Indies, Kingston, Jamaica, were invited to participate in a prospective studyinvestigating maternal determinants of fetal growth. Recruit-ment was restricted to women who were aged between 15and 40y, were 710 weeks pregnant, sure of their lastmenstrual period, and without systemic illnesses such aspre-eclampsia and diabetes, or genetic abnormality, forexample, sickle cell disease. Of the 712 women recruited,

569 completed the study. The other 143 were lost to thestudy for a variety of reasons. In all, 82 experiencedpregnancy losses, 56 withdrew for reasons such as workconstraints, migration or fear that ultrasonography wouldharm their fetus, and there were five sets of twins. All womenwere offered transportation to and from the hospital toenhance participation in the study. For this report, dataanalysis was confined to the 374 women on whommeasurements of placental volume at 14, 17 and 20 weeksgestation were complete.

Three individuals, MT, a nurse and a medical technologist,made all measurements. Two of the three observers made theultrasound measurements (MT and the technologist). Allthree were trained to apply the questionnaires and make themeasurements. At the start, and at three monthly intervalsfor the duration of the study, inter- and intraobservermeasurement variability were assessed, and training andrecertification prescribed for any observer whose scores werenot acceptable (Thame et al , 2000). Inter- and intraobservervariability for ultrasound measurements had a correlationcoefficient greater than 0.99 throughout the study. Smoking,alcohol and drug use were determined from questionnaireresponses, and a rating scale, based on social amenities andpossessions was used to define socioeconomic status (For-rester et al , 1996; Thame et al , 2000). The Ethics Committeeof the Faculty of Medical Sciences, The University of theWest Indies approved the study.

At each visit, maternal weight was measured to the nearest0.01kg using a Weylux beam balance (CMS WeighingEquipment Ltd, London, UK), height to the nearest 0.1cmusing a stadiometer (CMS Weighing Equipment Ltd, Lon-don, UK) and blood pressure with an oscillometric sphyg-

momanometer (Dinamap TM monitor Model 8100, CritikonInc.). Hemoglobin was measured with a Coulter counter(Coulter Electronics, Inc.) at the first visit.

Sonographic measurements (linear probe, ATL UltramarkIV; Advanced Technology Labs, Bothell, WA, USA) of fetusand placenta were made at 14, 17, 20, 25, 30 and 35 weeks of gestation to determine the changes in size with gestationalage. The method used to measure placental volume requiredthat the entire placenta be seen on the screen. After 20 weeksgestation, many placentas are too large for this, so placentalvolume was measured at only the first three visits; fetalbiparietal diameter, femoral length, and head and abdominalcircumferences were measured at all six visits. The average of

three repeats was used for each measurement. Placentalvolume was measured by identifying and recording onvideotape, the long axis of the placenta. A continuousrecording of the image of the placenta orthogonal to the axiswas made by sweeping the probe along the axis at constantvelocity. This axis was divided into six sections of equallength; the five interior cross-sectional areas were measuredand integrated to estimate the placental volume. Thismethod was developed and validated by Howe et al (1994).

Multiple linear regression and comparison of means wereused to analyze the data. Placental volumes were right-

Fetal growth and maternal anthropometryM Thameet al

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skewed, and thus, were square-root transformed to normal-ity. They were then adjusted for gestational age. Weight gainin early pregnancy between the first antenatal visit (810weeks) and 20 weeks gestation, the rate of growth of theplacenta between 14 and 17 weeks and 17 and 20 weeksgestation were calculated. Maternal weight at the firstantenatal visit, weight gain in early pregnancy, gender andgestational age were the main independent variables used inregression analyses. In the regression models, fetal measure-ments (abdominal circumference, femoral length, headcircumference and biparietal diameter) at 35 weeks gestationwere the dependent variables. The hypotheses being testedwere that maternal weight at the first antenatal visit, weightgain, placental volume and the rate of placental growth inearly pregnancy are related to sonographic measurements of fetal dimensions.

ResultsMean maternal measurements of the study group at 63 7 6days gestation are given in Table 1. The 338 women who

failed to complete the study were no different in age oranthropometry from the 374 women who did form the basisof this report (data not shown). Hemoglobin concentrationwas not available for 14 women, and blood pressuremeasurements were not successfully made in five patients.There was also no difference in newborn anthropometrybetween the two groups (data not shown). Mean neonatalmeasurements are shown in Table 1. Ten women in the studyhad pregnancy losses and nine women migrated, accountingfor the difference between the number of maternal measure-ments and birth weight seen in Table 1. As expected, fetaland placental measurements gradually increased throughoutpregnancy (Table 2). Also, it appears that ultrasoundmeasurements are a reasonable index of fetal growthcompared to measurements made at birth. Correspondingly,abdominal circumference at 35 weeks is highly positivelycorrelated with birth weight ( r 0.62, P o 0.001), and placen-tal volume measured at 20 weeks is highly positivelycorrelated with placental weight ( r 0.46, P o 0.001).

In order to explore the relationships between maternalweight and placental volume, the women were stratified intogroups of maternal weight, beginning at r 55kg andincreasing by 10kg, based on maternal weight at the firstantenatal visit. Those with lower maternal weight had asignificantly smaller placental volume at 17 and 20 weeksgestation ( P o 0.002 and o 0.0001, respectively) compared towomen with higher maternal weight (Table 3 and Figure 1).Similarly, there was a direct relationship between maternalbody mass index and placental volume at 14, 17 and 20weeks gestation. Hence, a 1 kg/m 2 increment in mothersbody mass index (BMI) at booking is associated with a 0.08(95% CI 0.010.14)-unit increase in the square root of

placental volume at 14 weeks gestation ( P 0.02); with a 0.07(95% CI 0.010.13)-unit increase at 17 weeks ( P 0.026);and with a 0.1 (95% CI 0.040.16)-unit increase at 20 weeks( P 0.001).

The simultaneous contributions of maternal weight andweight gain to fetal growth were also explored. Bothmaternal weight and maternal weight gain were stratifiedinto groups, and were directly related to fetal abdominalcircumference at 35 weeks. In any category of maternal

Table 1 Maternal and newborn characteristics

Variables Mean s.d. Range n

First Antenatal Visit Weight (kg) 65.5 13.1 32.9114.4 374Height (cm) 163.5 163.5 144.5182.8 374Body mass index (kg/m 2 ) 24.5 4.6 14.837.9 374Hemoglobin (g/dl) 12.2 1.1 8.815.5 360Systolic blood pressure (mmHg) 109.5 9.8 87.3140.7 369Diastolic blood pressure (mmHg) 63.0 7.9 40.784.7 369Gestational age (days) 63.0 6.0 4684 374

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

Table 2 Fetoplacental measurements from 14 to 35 weeks gestation

Gestation (weeks)

14 17 20 25 30 35

Variable Mean s.d. Mean s.d. Mean s.d. Mean s.d. Mean s.d. Mean s.d.

BPD (mm) 28.8 (371) 3.2 38.9 (373) 3.3 48.6 (372) 3.3 64.1 (321) 3.6 77.7 (318) 3.6 87.2 (309) 3.4HC (mm) 98.5 (371) 12.2 137.2 (372) 11.8 173.6 (373) 12.1 229.7 (321) 12.4 276.9 (318) 12.4 309.4 (309) 11.7 AC (mm) 85.9 (366) 11.4 120.0 (372) 11.1 152.6 (373) 11.9 206.9 (322) 14.4 262.8 (318) 16.8 314.6 (309) 18.6FL (mm) 15.0 (369) 3 24.6 (372) 3.1 33.6 (372) 2.9 46.7 (322) 3.1 58.4 (318) 3 68.9 (308) 3.2PV (ml) 116.5 (374) 52.3 242.9 (374) 73.4 359.8 (374) 84.5

Number of subjects within the brackets. BPD biparietal diameter; HC head circumference; AC abdominal circumference; FL femoral length; PV placentalvolume.


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weight, maternal weight gain was directly related to fetal

abdominal circumference (Table 4). Thus, women whosefetuses had the largest abdominal circumference were thosewho were heaviest at the first antenatal visit and gained thegreatest amount of weight in early pregnancy (Table 4). Thisanalysis was repeated for the other three fetal measurements,biparietal diameter, head circumference and femoral length,and similar results were obtained (data not shown). Placentalvolumes at 14, 17 and 20 weeks gestation were highlycorrelated, therefore, the earliest measurement (14 weeks)

was used in the regression analysis. Both gender andgestational 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 fetalmeasurements (biparietal diameter, femoral length, abdom-inal and head circumference). Placental volume at 14 weeksgestation and the rate of growth of the placenta between 17and 20 weeks gestation were significantly related to all fourfetal measurements. In further analyses when placentalvolume at 20 weeks gestation was added to the model, the14-week placental volume still independently contributed tofetal growth at 35 weeks gestation (data not shown). The rateof growth of the placenta between 14 and 17 weeks gestationwas significantly associated with fetal abdominal circumfer-ence and the femoral length at 35 weeks gestation.Abdominal circumference was the only fetal measurementthat was significantly associated with maternal weight at thefirst antenatal visit. Weight gain early in pregnancy wasassociated with all fetal measurements except femoral length.

The fetal measurements made were not associated withmaternal socioeconomic status. Less than 1% of mothersreported the use of alcohol or tobacco, and none admitted tothe use of illegal drugs.

DiscussionThis study reports on the inter-relationship of first trimestermaternal weight, subsequent weight gain in pregnancy,

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

r 55 118 46.9 227.6 70.7 330.7 80.9 7955.165.0 110.2 52.3 236.9 72 353.5 83.4 11865.175.0 115.9 54.1 247.7 76.2 374 94.3 894 75.1 124.4 54.7 259.9 71.9 380 70.4 88Total 116.5 52.3 242.9 73.4 359.8 84.5 374P 0.17 0.002 0.0001

Figure 1 Lines were drawn using the mean values of early weightgain between the respective dates of measurement; sex of child isfemale; parity is in the third quartile.

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) r 55 55.165.0 65.175.0 4 75.1 Total

r 0.5 297.8 (6) 309.5 (18) 302.3 (23) 317.5 (26) 309.1 (73)0.511.00 299.4 (14) 316.1 (20) 314.4 (13) 315.5 (16) 311.9 (63)1.001.50 313.7 (20) 315.8 (25) 310.6 (16) 318.2 (10) 314.4 (71)4 1.50 310.4 (24) 318.0 (31) 326.3 (24) 327.5 (23) 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 o 0.001 for maternal weight (kg) at the first antenatal visit on fetal abdominal circumference at 35 weeksgestation. [2] P -value for trend o 0.001 for early weight gain (kg/4 weeks) on fetal abdominal circumference at 35 weeks gestation.


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placental volumes in early pregnancy and fetalgrowth. In previous reports, birth weight and anthropo-metry at birth have been the outcome variablesmeasured and a positive relationship between maternalweight and birth weight has been reported (Kramer 1987;Thame et al , 1997; Kirchengast & Hartmann, 1998). Inthe present study, maternal first trimester weight andweight 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, femorallength, head and abdominal circumferences. The measure-ments at 35 weeks gestation were chosen as the outcomevariables, as in previous analyses (data not shown), associa-tions of maternal weight and fetal measurements were notseen until the 25th week of gestation. In assessing therelationships of placental volume and maternal weight gainin early pregnancy with fetal measurements, the lastrecorded fetal measurement, which was at 35 weeks gesta-tion, was used.

Low maternal weight in the first trimester, a proxymeasure of poor nutritional status, was associated with asmaller placenta and a smaller fetal abdominal circumfer-

ence at 35 weeks gestation. Maternal weight gain in earlypregnancy proved to be a more important predictor of fetalsize than maternal weight at the first antenatal visit. All fetalmeasurements except femoral length showed a significantpositive association with weight gain early in pregnancy andwomen who had a lower rate of weight gain deliveredsmaller babies than mothers who had a higher rate of weightgain. In previous studies, weight gain in pregnancy has alsobeen shown to be an important contributor to birth weight(Abrams & Selvin, 1995). It is possible that this influence onfetal size could be exerted through the adequacy of

placentation and indeed, lighter mothers had a smallerplacental volume at every stage of pregnancy.

The placenta is established early in intrauterine life, and itsrapid growth in the early part of pregnancy is important forthe supply of the nutrients necessary to ensure adequate fetalgrowth. The placenta exerts its effects on the growth of thefetus from the beginning of pregnancy by way of itstransport, metabolic and endocrine functions (Anthonyet al , 1995). The growth trajectory of the placenta isinfluenced by maternal size and nutrition before and during

early pregnancy and the rate of growth of the organ isinitially greater than that of the rate of growth of the fetus(Hendricks, 1964), in order to prepare the supply linenecessary for fetal growth.

This study also examined the effects of placental volumein early pregnancy, and the relationship between the rate of placental growth between 1417 and 1720 weeks gestationand fetal size. Although other studies have examined theeffect of placental volume on birth weight (Wolf et al , 1989;Clapp et al , 1995; Thame et al , 2001), this study contributesimportant information on the effect of placental volume aswell as the rate of placental growth in early pregnancy onfetal size (Clapp et al , 2000, 2002). Placental volume at 14

weeks gestation showed a significant positive associationwith all fetal measurements. Although the rate of growth of the placenta between 14 and 17 weeks gestation was animportant determinant of abdominal circumference andfemoral length, it was the rate of growth of the placentabetween 17 and 20 weeks gestation that showed significantpositive associations with all of the fetal measurements. Thismay imply that this period of gestation is important indetermining fetal size.

Smaller babies at birth are thought to be at increased riskfor chronic disease in adult life (Barker, 1997; Leon et al ,

Table 5 Maternal weight at the first antenatal visit, early weight gain, placental volume, rate of placental growth and fetal measurements at 35 weeksgestation: multiple regression analysis

Outcome variables are fetal measurements at 35 weeks gestation (mm)

Abdominal circumference Femoral length Head circumference Biparietal diameter

Variable B SEB B SEB B SEB B SEB

Gender (male 1, female 2) 2.09 1.77 0.08 0.32 4.14 1.26 w 0.83 0.35*Gestational age at 35 weeks gestation (days) 1.11 0.16 z 0.23 0.03 z 0.43 0.11 z 0.18 0.03 zPlacental volume at 14 weeks (s.d.)(ml) 8.34 1.15 z 1.09 0.21 z 3.33 0.82 z 1.10 0.23 zRate of placental growth between 14 and17 weeks gestation (ml/day)

102.80 22.65 z 11.82 4.10 w 27.69 16.17 7.56 4.44

Rate of placental growth between 17 and20 weeks gestation (ml/day)

98.35 21.79 z 14.58 3.95 z 36.52 15.56* 13.52 4.28 w

Maternal weight (kg) at the first antenatal visit 0.19 0.07 w 0.01 0.01 0.04 0.05 0.02 0.01Early maternal weight gain (first antenatalvisit20 weeks gestation) (kg/4 weeks)

4.35 0.99 z 0.19 0.18 1.61 0.70* 0.52 0.19 w

Constant 27.8 39.00 10.55 7.03 204.51 27.84 43.76 7.66 Adjusted R2 33.4 25.0 14.9 21.2

B is the regression coefficient. * P o 0.05; wP o 0.01; zP o 0.001.


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1998), and this study has shown that maternal nutrition, asmeasured by maternal weight and the rate of maternalweight gain in pregnancy, influences fetal size and hencebirth weight (Thame et al , 2001). Placental volume and therate of placental growth are also influenced by maternalweight, and in turn, also contribute to fetal size. Oneimplication of these results is that by securing catch upweight in undernourished mothers, it may be possible toimprove fetal growth. Such a finding would hold importantpublic health implications.

In conclusion, this study has provided evidence of asignificant influence of both placental volume, and the rateof placental growth, in determining fetal size and ultimately,birth weight. These effects appear to be mediated throughmaternal weight and weight gain in pregnancy and suggestthat these events determining fetal size operate early inpregnancy.

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