biological aspects - ADC Fetal & Neonatal Edition

FIO Archives ofDisease in Childhood 1996; 74: F10-F15

Fetal growth velocity: kinetic, clinical, andbiological aspects

Enrico Bertino, Eliana Di Battista, Anna Bossi, Marco Pagliano, Claudio Fabris,Giorgio Aicardi, Silvano Milani

Neonatal Unit,University ofTorinoE BertinoC Fabris

Institute ofPuericulture andNeonatal Medicine LGaslini, University ofGenovaE Di BattistaG Aicardi

Institute ofMedicalStatistics andBiometry, UniversityofMilanoA BossiS Milani

Department ofObstetrics andGynaecology,University ofTorinoM Pagliano

Correspondence to:Anna Bossi, Istituto diStatistica Medica eBiometria, Universita diMilano, Via Venezian 1,1-20133 Milano, Italy.Accepted 9 August 1995

AbstractWith the aim of determining fetal growthkinetics, prenatal data were analysedwhich had been longitudinally collected inthe framework ofa perinatal growth survey.The sample comprised 238 singletonnormal pregnancies, selected in Genoaand Turin (between 1987 and 1990), andrepeatedly assessed by ultrasound scans(five to nine per pregnancy). Fivemorphometric traits were considered:BPD (biparietal diameter), OFD(occipitofrontal diameter), HC (headcircumference), FDL (femur diaphysislength) and AC (abdomen circumference).Growth rate seemed to increase in the

early part of the second trimester, anddecrease subsequently: velocity peakswere steeper and earlier for headdiameters and circumference (about 18weeks) than for femur length (20 weeks)and abdomen circumference (22 weeks).Velocity standards were traced using alongitudinal two-stage linear model: thisensures unbiased description of the shapeof the growth curve, even when growthkinetics are asynchronous, and efficientestimation ofthe outer centiles - the mostuseful for diagnostic purposes.(Arch Dis Child 1996; 74: F1O-F15)

Keywords: fetal growth velocity, head diameters, headand abdomen circumferences, femur length.

Before the development of ultrasonography,there was no harmless and reliable techniqueavailable for providing information on physio-logical fetal growth kinetics, and the so-calledintrauterine growth standards were thereforebased on anthropometric measures ofneonateswith different gestational ages. As the assump-tion that prenatal growth in full term andpreterm babies follows the same pattern ishardly tenable,' these norms are intrinsically atool for evaluating body size and proportion ofneonates, and not true growth standards formonitoring fetal development.2

Unfortunately, most ultrasonographicnorms derive from cross-sectional surveys,-5or from longitudinal surveys involving either alimited number of observations per pregnancyor a limited number of pregnancies.610 Evenin the case of longitudinal studies, data aregenerally processed as coming from cross-sectional surveys, so that the specific possi-bilities of these studies (such as the estimationof growth velocity and the analysis of thepattern of growth) are overlooked and lost.

In this paper we present a new kinetic modelfor fetal growth and velocity charts computedon a large sample of pregnancies, collected andrepeatedly assessed by ultrasound scans in theframework of a prospective perinatal growthlongitudinal survey.

MethodsPregnant women were selected in Genoa andTurin, between 1987 and 1990, in accordancewith the restrictive criteria recommended byFIGO,1 1 so as to include only normal singletonpregnancies. The sample so obtained com-prised 238 neonates (123 girls, 115 boys)delivered at term after low risk, uncomplicatedpregnancy. Gestational age was estimated fromthe last menstrual period and was confirmedby an early ultrasound assessment ofcrown-rump length'2 performed within the12th week: when the difference between thetwo estimates exceeded seven days, the preg-nancy was excluded from the reference set.Informed consent was obtained from eachwoman participating in the survey.

Individual growth profiles consist of five tonine measures (totalling from 1539 scans forbiparietal diameter, to 1237 scans forabdomen circumference), taken between the12th and the 40th gestational week. Allmeasurements were performed by four trainedechographers, using real time scanners(Ansaldo AU920, ATL Ultramark IV, ToshibaSAL 30A) equipped with 3*5 MHz trans-ducers. In accordance with the methoddescribed by Campbell,13 BPD (biparietaldiameter) was measured at the largest trans-verse diameter ofhead at the level of thalamus,from the outer edge of the proximal skull tableto the inner edge of the distal skull tables,whereas OFD (occipitofrontal diameter) wasobtained from middle to middle measurementson the same plane used for BPD.14 HC (headcircumference) was computed from the shortand long axes of head taken from the outercontour of skull profile.'5 FDL (femurdiaphysis length) was determined as the largestof three measures obtained according toQueenan et al.'6 AC (abdomen circumference)was computed from the antero-posterior andtransverse abdomen diameters, measured astwo perpendicular axes of the outer contour ofabdomen profile at the level of the medianportion of porto-umbilical vein passingthrough the liver, as indicated by Kurjac andBreyer. 17A test-retest experiment was performed to

estimate the comparability ofmeasurements. Aset of 20 pregnant women with pregnancies

on June 27, 2022 by guest. Protected by copyright.

http://fn.bmj.com

/A

rch Dis C

hild Fetal N

eonatal Ed: first published as 10.1136/fn.74.1.F

10 on 1 January 1996. Dow

nloaded from

http://fn.bmj.com/

Fetal growth velocity Fll

4.0 - Biparietal diameter

3.5

3.0

(D

2.5 _-EE

2.0-

.=1.5-

1.0

-5th/95th-lO--1th/90th cetl0.5 ---- 25th/75thrcetl

50th J

0.0 I12 16 20 24 28 32 36 40

Gestational age (weeks)Figure 1 Standards ofBPD (biparietal diameter) growthvelocity (mm/week) as a function of menstnral age(weeks). The chart applies to estimates ofgrowth velocitybased on measures taken six weeks apart.

ranging from 13 to 36 weeks (the same numberof pregnancies in the second and in the thirdtrimesters), were independently examined bytwo echographers. The average measuringerrors (mm), expressed as smeans and concern-ing the second and the third trimester, respec-tively, were as follows: 0-67 and 0-76 (BPD),1-26 and 1-46 (OFD), 2-43 and 3 49 (HC),0-74 and 0-88 (FDL), 4-02 and 6-44 (AC).

STATISTICAL METHODSGrowth functionsMost of the mathematical functions used tomodel prenatal growth of BPD and other onedimensional traits belong to the same family ofthree constant linear growth functions:

loge{yi(t) } =tOi+a-ifl (t) +x2if2i(t) +ei(t)Where yi(t) is the value of the trait measuredon the i-th individual at age t; Ei(t) is the intra-individual random term associated withloge{yj(t)}; ooi) ali, and a2i are the growthconstants of the i-th individual; lastly fi (t) andf2(t) are selected functions of age which deter-mine the shape of growth model. If we setfi(t)=t and f2(t) =loge(t) we get a Count func-tion'8 in a log scale (we shall call it log countfunction). The logarithmic form of Rossavik-Deter'9 and Todros et a14 exponential-powerfunctions may be derived by log-Countfunction if we set f, (t) =tXloge(t) and a22=2,respectively. All these functions have a pointof inflection4 19 but do not have an upperhorizontal asymptote, thus allowing for the factthat fetal growth velocity increases moderatelyin the first months of gestation, and thendecreases slowly without falling to zero.20The comparison of the functions mentioned

above on the basis of the analysis of residuals

and of the precision of the estimates indicatedthat Todros et al (for AC) and log-Count func-tions (for the remaining traits) led to the mostsatisfactory description of fetal growth: themaximum systematic departure of these func-tions for the growth profile was less than 3%.21The analysis of fetal growth kinetics andvelocity standards presented are based on thesefunctions.

Two-stage models and longitudinal standardsThe fitting of appropriate functions to indi-vidual growth profiles may be regarded as thefirst stage of an explicit two-stage model.22 Inthis first stage the individual growth constantswere estimated by ordinary least squaresmethod, under the usual assumptions that theintra-individual component of variance (whichaccounts for both measurement error and bio-logical random fluctuations due to variations ofthe intrauterine environment and to nutritionalfactors) is nearly the same over time andsubjects, and that repeated measures areuncorrelated. In the case of intrauterinegrowth these assumptions seem to be sensibleand fairly consistent with empirical evidence,provided that a log scale is adopted,homogeneous reference groups are selected,and a flexible growth function (such as the log-Count function defined here) is fitted todata.21

In the second stage the average growth con-stants (which express the mean growth patternof the reference population) and the inter-individual covariance matrix (which expressesdifferences between the individual growthpatterns of fetuses belonging to the same refer-ence group) were simultaneously estimated byan expectation maximisation interactive algo-rithm (Milani S, Bossi A, Marubini E. Papercontributed to 46th Session of InternationalStatistical Institute, Tokyo, 1987) which leadsto generalised least squares estimates. Thismethod allows for the fact that individualgrowth constants are estimated from observa-tions which differ in number and time loca-tion.Growth velocity charts (the centiles of the

distribution of the growth velocity of a giventrait conditional on gestational age) werederived from the above average growth con-stants and interindividual covariance matrix,under the hypothesis that the measures aretaken six weeks apart for BPD, OFD, HC, andFDL, and 10 weeks apart for AC: because ofmeasurement errors, velocity values computedon shorter time intervals are too unreliable tobe of practical use (see the appendix for thealgebraic details).

ResultsFigures 1-5 show growth velocity standards forBPD, OFD, HC, FDL, and AC. For all thesetraits, growth velocity seemed to increase in theearly part of the second trimester and decreasesubsequently up to the end of pregnancy.Interindividual variability of growth velocitychanges remarkably with gestational age: it


http://fn.bmj.com

/A

rch Dis C

hild Fetal N



nloaded from

http://fn.bmj.com/

F12 Bertino, Di Battista, Bossi, Pagliano, Fabris, Aicardi, Milani

Figure 2 Standards ofOFD (occipitofrontaldiameter) growth velocity(mm/week) as a function ofmenstrual age (weeks). Thechart applies to estimates ofgrowth velocity based onmeasures taken six weeksapart.

5 5 Occipito-frontal diameter

5-0 _ ..--..

4.5

4.0

1~0 _ ------5h9th.'

353.E

E53.0 \

o 2.5 -

20(.9 1.5-

1.0 --5th/95thlO--1th/90thcetl

0.5 25thf75th cetl50th

12 16 20 24 28 32 36 40Gestational age (weeks)

rises up to the peak ofvelocity, lessens reachinga minimum between 25 and 30 weeks ofgestation, and then increases again up to theend of the pregnancy.

Different morphometric traits displaydifferent ages at the peak of growth velocity.The peak of velocity occurs earlier in headmeasurements (BPD: 17-9 completed weeks(SE 015), OFD: 17A4 (0-13), HC: 17-3(0.11)), and later for FDL (20-2 (0.13)) andAC (22d1 (0 27)). Furthermore, the change ofvelocity with age is less for AC than for headdiameters and circumference, while is some-what more prominent in FDL. The above

16Head circumference

14-

12

2 _:. _--10t/0h cnie '\

10 1

E

0

-C 6-

-Figr sth/95th c

2 -----1th/90th Letl25th175,th cete

velocity (mm/week) as a function of menstrual age(weeks). The chart applies to estimates ofgrowth velocitybased on measures taken six weeks apart.

differences in the pattern ofgrowth of the traitsunder study are shown in figure 6, where thevelocity of each trait is expressed as a percent-age of its size at 40 gestational weeks. In thesame figure the growth velocity of cubic BPD(which is roughly proportional to headvolume) is also shown: the peak velocity issharper and takes place much later (31-1 weeks(0 27)) for computed head volume than forhead diameters and circumference.

Only minor differences in the growthpattern of one dimensional traits emergedbetween sexes: differences seemed to be negli-gible from a clinical point ofview and could beignored in drawing prenatal growth velocitycharts.

HEADThe estimated value of gestational age at peakof velocity was about 17-18 weeks for BPD,OFD, and HC. Lower values were derivedfrom the mixed longitudinal study (13-16weeks) of Guihard-Costa et al 10 and from thecross-sectional study (16-4 weeks) of Todroset al.4 Higher values (20-8 weeks) are reportedby Erikssen et al 23 on the basis of a longitudi-nal study. Similar velocity values and analo-gous decrease of velocity after the 17thgestational week were observed by Campbellet al 6 in a longitudinal study (191 pregnancies,3X4 scans/pregnancy): however, in their studythe age at peak could not be estimated,because of the lack ofmeasurements before the17th week. Jeanty et al 24 and Munjanja et al 25observed that growth velocity increases after14-15 gestational weeks. From the longitudi-nal observation of 30 pregnancies, Fescinaet al 26 infer that the maximum growth velocityof intracranial perimeters occurs between the14th and the 16th gestational weeks. Deteret al,27 in the first longitudinal study aimed tomodel fetal growth, and which involved only20 pregnancies, observed that BPD growthcurve has a slight upward convexity which con-tinues up to 38 weeks of gestation, whereasHC is characterised by a linear phase up to 30weeks and by a subsequent slow down ingrowth velocity. Ten years later, Deter andHarrist28 observed that HC growth ratedecreases from 14 mm/week (at 14 weeks ofgestation) to 9 mm/week (at 30 weeks) and5 mm/week (at 38 weeks).Our data indicate that peak growth velocity

for BPD, OFD, and HC occurs at the end ofthe first phase of rapid increase in forebrain cellnumber, when major neuronal proliferationoccurs. The subsequent decrease in growthvelocity of these one dimensional traits doesnot necessarily reflect a contemporary slowdown in the weight gain of the brain (which isa complex three dimensional structure andapproximates the growth pattern of cubicBPD), whose peak growth velocity seems to belater than those of one dimensional traits.29Our findings agree with those of Meire,30 whopoints out that the growth curve of fetal headvolume has a shape rather different from thatof BPD, with a velocity decrease after 28-32weeks.


http://fn.bmj.com

/A

rch Dis C

hild Fetal N



nloaded from

http://fn.bmj.com/

Fetalgrowth velocity F13

Figure 4 Standards ofFDL (femur diaphysislength) growth velocity(mm/week) as affunction ofmenstrual age (weeks). Thechart applies to estimates ofgrowth velocity based onmeasures taken six weeksapart.

,_ Femural diaphysis length

30 1 2 8

2.5-0 7

At5-rsn 10hre teaientlyewaasialformoelling thegroth kntc ftefmr12we 12 2422 32 36 40

morerecentstuyEationaloaetalwe noicetha

FEMU

grothprsen therly lnare frelatvel few dat suitsable

thenmodeli 5the/ growth velocity0ano5b estimth/d tfro cetheicrs-etoa

Onthbasisaoflongitudinal observations,crieu

by~ ~~25h7tEljleadD ljle9sgettagrowthnaf ethe alfemst tht islinearbtween 12angestationa22 s age (weeks) es t

foremeletl nbth growthkineti anothcemu.ha

OntebssoLongitudinaldaarpreyO'Bsrvaions,taQuenarns et al7stat thspatiiagrowthislna

bewe11 n2 weeks of gestation,rsetvl. InlamoihredrCentstudaxcosoeta1°onteai not icedta

growth is fairly linear from 13 to 28 weeks andthen slows down, even if growth velocitycannot be estimated from their cross-sectionaldata. Cross-sectional data reported by Yehet al 3 and longitudinal observations carried outby Elejalde and De Elejalde,9 suggest thatgrowth ofthe femur is linear between 10 and 40weeks of gestation: but such a patten seems tobe unusual for any biological growth process.3'Longitudinal data reported by O'Brien et a18and Brons et a132 display similar growthpatters with a decrease in velocity after 17 and12 weeks of gestation, respectively. OnlyGuihard-costa et al,'0 on the basis of mixedlongitudinal data, observe a non-monotonickInetic pattern, with a peak between 13 and 16weeks and a subsequent decrease in velocity.From our longitudinal study it emerged that

FDL growth velocity peaks at about 20 weekswhen, according to Tanner,33 the peak ofvelocity in fetal crown-heel length occurs,which is highly correlated with femur length.

ABDOMENAs to growth of abdomen circumference., theage at peak estimated from our study (22weeks) is higher than those reported byGuihard-Costa et al'10 (from 13 to 16 weeks)andt Todiroset al4 (20 weeks), buit lowe-r thann

of gestation) to 11 mm/week (by the 38thweek).Our analysis indicates out that the variations

in AC growth velocity during prenatal life areless prominent than those of head and femur,which agrees with the findings of Erikssen et al23 and Meire,30 who remark that AC growth ismore linear than that of the other traits. ACreflects, to a large extent, the size of the liverand the thickness of subcutaneous fat tissuewhich grow mainly in the last trimester ofpreg-nancy,34 35 and is reported as a trait useful toestimate fetal weight.17 However, the peak ofAC growth velocity comes far earlier than thatof body weight, which is supposed to occurbetween 34 and 38 weeks of gestation.33 Thistime lag may be explained by several factors.

First, one dimensional traits progress arith-metically throughout gestation, while weight,which is proportional to volume, progressesgeometrically, rather like cube BPD. Secondly,abdomen circumference mainly reflects thetransversal size of the liver, and not its volume,whose exponential growth is similar to that ofbody weight.36 Finally, more subcutaneous fat,which contributes predominantly to bodyweight during the third trimester ofpregnancy,is stored in limbs and subscapular sites than inthe abdomen.37

DIFFERENCES BETWEEN FETAL GROWTHKINETICSIn our study the peak of AC growth velocityoccurred just after the end of adipose tissueappearance in the abdominal wall where thishappens earlier than in the limbs.38 At variancewith the findings outlined by Guihard-Costaet al,'0 in our study a prominent differenceemerged between the ages at peak velocity forhead, femur, and abdomen. In fact, it is widely

13 Abdomen circumference

12

11

-) 10

E --,E 9 /

18

6-----5th/95th

-ohvoi O10th/90th enctile5 - 25th/-75thcete

baseon easGestational0 ageks(weeks)


http://fn.bmj.com

/A

rch Dis C

hild Fetal N



nloaded from

http://fn.bmj.com/

F14 Bertino, Di Battista, Bossi, Pagliano, Fabris, Aicardi, Milani

Figure 6 Mean growthvelocity (as per cent of thesize attained at 40 weeks)as a function of menstrualage (weeks). Head volume(HHV) was regarded asproportional to cubic BPD.

5 5 _ HVFDL

5.0 --SPDOFD

BPD

4.0

Q3.5-

10

2,5

-~2.0

1.5-

1.0

0.512 16 20 24 28 32 36 40

Gestational age (weeks)

known that fetal growth is characterised bydifferent rates for organ weight and size, limblength and head circumference and volume, sothat body shape and proportions change overgestation.39 On the other hand, differences infetal growth kinetics of head and abdomencircumferences emerge also from the inspec-tion of preterm and full term babies: pretermneonates have a ratio of head and brain size tobody mass that is larger than that of full termneonates, and this may account for their veryhigh glucose turnover.40 Anoxia affecting fetaldevelopment in the first four months of gesta-tion results in generalised growth impairment(weight, length, and head size), while anoxiaoccurring in the last months of pregnancyaffects mainly weight and results in a low birth-weight baby with normal head circumferenceand length.4

DiscussionIntrauterine growth velocity has a non-monotonic pattern: it increases in the first partof pregnancy and decreases in the last part.The age at peak velocity as well as the extent ofthe peak depend on the morphometric traits:peaks are sharper and occur later for threedimensional traits than for one dimensionaltraits. Furthermore, abdomen circumferencereaches maximum growth velocity two weeksafter femur length and five weeks after headcircumference. The reliability of these con-clusions rests on the number of records perlongitudinal profile (from five to nine,mean=6-5), the size of sample (238 preg-nancies), the strictness of criteria adopted toselect normal pregnancies resulting in normaloutcome, and the relatively good precision ofultrasonographic measurements.The velocity standards presented here are

entirely based on a two-stage linear model. Inthe first stage the individual intrauterinegrowth profiles were fitted by a proper growth

function: Todros et al 'S4 function for AC and anew function derived from Count's function18for the other fetal traits (log-Count function).The systematic discrepancies which emergedbetween observed and fitted values (less than3%) are negligible from a clinical viewpoint.The second stage implied the estimate of themean constant curve and of the covariancematrix which expresses interindividual vari-ability, required to compute growth centiles.Using this method, the shape of velocity curvecan be described without bias, even whengrowth kinetics are not synchronous amongindividuals, and efficient estimates are attainedeven for the outer centiles which are the mostuseful for diagnostic purposes. Unfortunately,the precision of the current ultrasonographictechniques is still inadequate to obtain reliablemeasures of individual growth velocity onshort time intervals. This drawback restrictsthe practical use of velocity charts to velocityestimates derived from measures taken at leastsix (for BPD, OFD, HC, and FDL) or 10 (forAC) weeks apart.

AppendixLet us consider a morphometric trait (y) whoseexpected growth in a given subject is describedby a continuous function of time (t). Thisfunction is characterised by a vector of indi-vidual parameters a which, in the populationfrom which the subject has been drawn, is arandom variable with mean vector i andcovariance matrix I

E(yla)=f{a;t} E(y)=f{f;t} V(a)=2G (1)

Therefore, a single measure y taken on thesubject at time t may be expressed as

y=f{a,E;t} =f{jP,(X-{),E;t} (2)

where random terms (ao-A) and E account forinterindividual and intra-individual variability.The fetal growth models (log-Count functionand Todros et a14 functions) on whichstandards here presented are based may bewritten as:

y=exp{q' +q'(a{A)+E} (3)

where g'={1, t, loge(t)}. Under the usualassumption for random terms (ie, V(E)=92=,Cov(Ei,Ej) =0, and Cov{q'(ao-),E}=0, the vari-ance of a new observation (y) at time t, pre-dicted on the basis ofan unbiased estimate A off, is given by the sum of the interindividualand intra-individual components,42 and maybe computed (approximately) from equation 3by means of a Taylor series expansion aboutf{ji;t}

V($-[V{fit}]2x { [q'(^,~+V(c))q] +u2} (4)

Let us denote the first derivative of vector g'respect to time t as 3g'={0, 1, l/t) and writethe expected individual growth velocity as:

E(v|a)=df{a;t}/dt=f{ac;t} X {ag'#+aq'(a-fi) } (5)


http://fn.bmj.com

/A

rch Dis C

hild Fetal N



nloaded from

http://fn.bmj.com/

Fetal growth velocity F15

The variance of a predicted value of velocity vis given by the sum of an interindividual com-ponent, which does not depend on the timeinterval At on which velocity is measured, andof an intra-individual component which doesdepend on At:

V(v)-V(E(VjoI))+ [{fi;t}]2X2U2/At2 (6)

where V(E(VIox)) may be computed (approxi-mately) from equation 5 by means of a Taylorseries expansion about f{fi;t}

V(E(VIa))-m[f{;t}]2X {(aq'pf'aq) X [q'(Ia+V(P))_q +

+[aq'(X0+V(A))q]+2X(aq' )x[g'(X,+V(fi))_q]} (7)

The estimate of V(v) was obtained by replace-ment of f, Xas V(p) by their generalised leastsquare estimates I,, V()22, and c by thepooled residual mean square error (s2) aboutthe individual growth curves.For all traits, the distribution of the fitted

values of individual growth velocities condi-tional on gestational age was close to thenormal distribution: this is not surprising, as allfetal traits under study are one dimensional.For this reason, the usual parametric estimatesof centiles were computed. As At, we chose aninterval of six weeks for BPD, OFD, HC, andFDL and an interval of 10 weeks for AC, themeasures of which seemed to be affected byrelatively larger errors. The choice was a com-promise between the size of technical error andthe obstetrician's need to have a ready assess-ment of the normality of fetal growth.We are deeply grateful to Professors J M Tanner and M J RHealy, whose valuable experience and incisive suggestionssupplied us with insight into the methodological aspects impliedin the construction of velocity standards.

Supported in part by Grants from Piemonte and Liguriaregions, and from Istituto G Gaslini, Genova.

Presented in part (as an abstract) at the 6th InternationalCongress of Auxology, Madrid, September 1991.

1 Falkner F. Perinatal growth. Arch Fran,c Pediatr 1985; 42:195-7.

2 Secher NJ, Kern Hansen P, Thomsen BL, Keiding N.Growth retardation in preterm infants. Br Jf ObstetGynaecol 1987; 94: 115-20.

3 Yeh MN, Bracero L, Reilly KB, Murtha L, Aboulafia M,Barron BA. Ultrasonic measurement of the femur lengthas an index of fetal gestational age. Am J7 Obstet Gynecol1982; 144: 519-22.

4 Todros T, Ferrazzi E, Groli C, Nicolini U, Parodi L, PavoniM, et al. Fitting growth curves to head and abdomenmeasurements of the fetus: a multicentric study. J ClinUltrasound 1987; 15: 95-105.

5 Exacoustos C, Rosati P, Rizzo G, Arduini D. Ultrasoundmeasurements of fetal limb bones. Ultrasound ObstetGynecol 1991; 1: 325-30.

6 Campbell S, Newman GB. Growth of the fetal biparietaldiameter during normal pregnancy. 7 Obstet Gynaecol BrCwlth 1971; 78: 513-9.

7 Queenan JT, Kubarych SF, Cook LN, Anderson GD,Griffin LP. Diagnostic ultrasound for detection ofintrauterine growth retardation. Am J Obstet Gynecol1976; 124: 865-73.

8 O'Brien GD, Queenan JT. Growth of the ultrasound fetalfemur length during normal pregnancy. Am J ObstetGynecol 1981; 141: 833-7.

9 Elejalde BR, de Elejalde MM. The prenatal growth of thehuman body determined by the measurement of bonesand organs by ultrasonography. AmJIMed Genet 1986; 24:575-98.

10 Guihard-Costa AM, Droulle P, Larroche JC. Growthvelocity of the biparietal diameter, abdominal transversediameter and femur length in the fetal period. Early HumDev 1991; 27: 93-102.

11 International Federation of Gynecology and Obstetrics.SubCommittee on Perinatal Epidemiology and HealthStatistics. Report on the methodology of measurement and

recording of infant growth in the perinatal period. London:FIGO, 1986.

12 Robinson HP. Sonar measurement of fetal crown-rumplength as means of assessing maturity in first trimester ofpregnancy. BMJ 1973; 4: 28-31.

13 Campbell S. An improved method of fetal cephalometryby ultrasound. J Obstet Gynaecol Br Cwlth 1968; 75:568-76.

14 Jeanty P, Romero R. Obstetrical ultrasound. New York:McGraw Hill, 1984.

15 Grannum PAT. Ultrasonic measurements for diagnosis. In:Gross TL, Sokol RJ, eds. Intrauterine growth retardation.A practical approach. Chicago: Year Book MedicalPublishers, 1989: 123-57.

16 Queenan JT, O'Brien GD, Campbell S. Ultrasoundmeasurement of fetal limb bones. Am Jf Obstet Gynecol1980; 138: 297-302.

17 Kuriac A, Breyer B. Estimation of fetal weight by ultrasonicabdominometry. Am Jf Obstet Gynecol 1976; 125: 962-5.

18 Count EW. Growth pattern of the human physique: anapproach to kinetic anthropometry. Part I. Hum Biol1943; 15: 1-32.

19 Rossavik IK, Deter RL. Mathematical modelling of fetalgrowth: I. Basic principles. Jf Clin Ultrasound 1984; 12:529-33.

20 Wiener SN, Flynn MJ, Kennedy AW, Bonk F. A compositecurve of ultrasonic biparietal diameters for estimatinggestational age. Radiology 1977; 122: 581-3.

21 Milani S. Modelling kinetics of somatic growth. In:DiBacco M, Pacciani E, Borgognini-Tarli S, eds.Statistical tools in human biology. London: World ScientificPublishing Company, 1994: 179-93.

22 Berkey CS, Laird NM. Nonlinear growth curve analysis:estimating the population parameters. Ann Hum Biol1986; 13: 111-28.

23 Erikssen PS, Secher NJ, Weis-Bentzon M. Normal growthof the fetal biparietal diameter and the abdominaldiameter in a longitudinal study. Acta Obstet GynecolScand 1985; 64: 65-70.

24 Jeanty P, Cousaert E, Hobbins JC, Tack B, Bracken M,Cantraine F. A longitudinal study of fetal head biometry.Am Jf Perinatol 1984; 2: 118-28.

25 Munjanja SP, Masona D, Masvikeni S. Fetal biparietaldiameter and head circumference measurements: resultsof a longitudinal study in Zimbabwe. Int Jf Gynecol Obstet1988; 26: 223-8.

26 Fescina RH, Ucieda FJ, Cordano MC, Nieto F, TenzerSM, Lopez R. Ultrasonic patterns of intrauterine fetalgrowth in a Latin American country. Early Hum Dev1982; 6: 239-48.

27 Deter RL, Harrist RB, Hadlock FP, Poindexter AN.Longitudinal studies of fetal growth with the use ofdynamic image ultrasonography. Am J Obstet Gynecol1982; 143: 545-54.

28 Deter RL, Harrist RB. Growth standards for anatomicmeasurements and growth rates derived from longitudinalstudies of normal fetal growth. Jf Clin Ultrasound 1992; 20:381-8.

29 Dobbing J, Sands J. Head circumference, biparietaldiameter and brain growth in fetal and postnatal life. EarlyHum Dev 1978; 2: 81-7.

30 Meire HB. Ultrasound measurement of fetal growthpatterns. In: Falkner F, Tanner JM, eds. Human growth.Vol 1. New York: Plenum Press, 1986:275-90.

31 Baily NTJ. The mathematical approach to biology andmedicine. XIV Series on quantitative methods of biologistsand medical scientists. London: Wiley, 1970.

32 Brons JTJ, van Geijn HP, Bezemer PD, Nauta JPJ, Arts NF.The fetal skeleton; ultrasonographic evaluation of thenormal growth. Eur J Obstet Gynaecol Reprod Biol 1990;34: 21-36.

33 Tanner JM. Foetus into man. 2nd edn. Welwyn Garden City:Castlemead Publications, 1989.

34 Murao F, Senoh D, Takamiya 0, Yamamoto K, HasegawaK, Kitao M. Ultrasonic evaluation of liver development inthe fetus in utero. Gynecol Obstet Invest 1989; 28: 198-201.

35 Micheli JL, Pfister R, Schutz Y, Calame A, Jequier E.Skinfold thickness and body composition during earlypostnatal growth in low birthweight infants. DevPhysiopathol Clin 1991; 2: 113-23.

36 Singer DB, Sung CJ, Wigglesworth JS. Fetal growth andmaturation with standards for body and organ develop-ment. In: Wigglesworth JS, Singer DB, eds. Textbook offetal and perinatal pathology. Vol 1. London: BlackwellScientific Publications, 1991:11-47.

37 Vaucher YE, Harrison GG, Udall JN, Morrow G. Skinfoldthickness in North American infants 24-41 weeksgestation. Hum Biol 1984; 56: 713-31.

38 Poissonnet CM, Burdi AR, Garn SM. The chronology ofadipose tissue appearance and distribution in the humanfetus. Early Hum Dev 1984; 10: 1-11.

39 Hata T, Deter RL. A review of fetal organ measurementsobtained with ultrasound: normal growth. J ClinUltrasound 1992; 20: 155-74.

40 Ogata ES. Carbohydrate metabolism in the fetus andneonate and altered neonatal glucoregnlation. Ped ClinNorth Am 1986; 33: 25-45.

41 Brar HS, Rutherford SE. Classification of intrauterinegrowth retardation. Semin Perinatol 1988; 12: 2-10.

42 Fearn T. A bayesian approach to growth curves. Biometrika1975; 62: 89-100.


http://fn.bmj.com

/A

rch Dis C

hild Fetal N



nloaded from

http://fn.bmj.com/

Documents

biological aspects - ADC Fetal & Neonatal Edition