Early Human Development 88 (2012) 473–478

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Early Human Development

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Longitudinal growth of head circumference in term symmetric and asymmetric smallfor gestational age infants

Harvinder Kaur, A.K. Bhalla ⁎, Praveen KumarDepartment of Pediatric Medicine, Advanced Pediatrics Centre, Postgraduate Institute of Medical Education & Research (PGIMER), Chandigarh, India

⁎ Corresponding author. Tel.: +91 712 2755307, +9E-mail address: anilbhalla@sify.com (A.K. Bhalla).

0378-3782/$ – see front matter © 2011 Elsevier Irelanddoi:10.1016/j.earlhumdev.2011.11.007

a b s t r a c t

a r t i c l e i n f o

Article history:

Received 10 March 2011Received in revised form 29 September 2011Accepted 3 November 2011

Keywords:Asymmetric SGAHead circumferenceLongitudinal dataSymmetric SGATerm infants

Aims: To study longitudinal growth pattern of head circumference of full-term symmetric and asymmetricsmall for gestational age (SGA) infants of the two sexes during first year of life.Study Design: Mixed-longitudinal growth research design.Subjects: Head circumference amongst full-term 100 symmetric, 100 asymmetric as well as 100 appropriatefor gestational age (AGA) infants was measured at birth, 1, 3, 6, 9 and 12 months of age using standardizedtechnique and instrument.Results: The mean head circumference of male symmetric SGA infants measured significantly (p≤0.001)smaller than asymmetric SGA infants while, in female symmetric SGA infants it measured shorter beyond6 months. As compared to AGA infants, head circumference in symmetric and asymmetric SGA infants mea-sured significantly smaller in size. Growth velocity for head circumference amongst symmetric and asym-

metric SGA male infants did not show statistically significant differences. Rate of head circumferencegrowth remained significantly higher amongst female asymmetric SGA infants than the symmetric ones be-tween 3 and 6 months while, a reversal of trend was observed between 9 and 12 months.Conclusion: The better growth attainments for head circumference of male and female asymmetric SGA in-fants than their symmetric SGA counterparts during first postnatal year of life may be attributed to the con-tinuation of influence of “head sparing” experienced by asymmetric SGA babies during prenatal life.

© 2011 Elsevier Ireland Ltd. All rights reserved.

1. Introduction

Depending on the timing and severity of insult, etiologically,small for gestational age (SGA) infants are classified into symmetri-cal (proportionate) and asymmetrical (disproportionate) pheno-types. Inhibiting factors like viral infections, inherited abnormality ofcellular development and chemical exposure which operate early inpregnancy (first trimester), yield symmetrically growth retarded fetus.Conversely, a late pregnancy insult leads to birth of a baby with asym-metric growth retardation [1,2]. In infants affected in first trimester, re-tardation will affect weight, length and head circumference (symmetricgrowth retardation). If the insult/nutritional deprivation occurs later inpregnancy the brain will be spared but length as well as weight will bedecreased, resulting into birth of a disproportionate baby (asymmetricgrowth retardation) [3,4].

Studies carried out in different parts of the world [5-9] revealedthat babies with symmetric growth retardation possessed smallerhead circumference than the asymmetric infants. However, longitudi-nal anthropometric data on head growth of symmetric as wellas asymmetric SGA babies of Indian origin as well as for other

1 9316102785.

Ltd. All rights reserved.

developing countries during the postnatal years are lacking whereSGA is relatively much more common, contributing to 77-90% of Indi-an LBW babies [10]. SGA infants besides exhibiting higher perinatal,neonatal and post neonatal mortality as well as morbidity rates[11,12] also have long-term adverse neurodevelopmental outcome[13-16]. Hence, to understand post-natal head growth dynamics ofboth symmetric as well as asymmetric SGA babies growing under a va-riety of environmental, nutritional, geographic and socio-economicconstraints and conditions prevailing in developing countries, in thispresentation an attempt has been made to study the pattern of thegrowth of head circumference of full-term symmetric and asymmetricSGA babies.

2. Material & Methods

2.1. Participants

A total of 200 full-term SGA (i.e. Symmetric SGA: boys 50 & girls50; Asymmetric SGA: boys 50 & girls 50) and 100 (boys, 50 & girls,50) full-term AGA babies born to parents representing upper middleto upper high socioeconomic strata [17] in the Labor Room of thePostgraduate Institute of Medical Education and Research (PGIMER),Chandigarh, India comprised the sample for the present study. The es-timation of sample size for this serial studywith one tailedα=0.05 and

474 H. Kaur et al. / Early Human Development 88 (2012) 473–478

power=95%was done by using Power and Precision ver. 2 Biostat, USA2000.

The babies born between 37 and 41 completed weeks of gestation(259–293 days) were designated as full-term [18]. Infants weighingwithin 10th to 90th percentile of intrauterine growth curves establishedby Lubchenco et al. (1963) [19] were treated as AGA, while thoseweighing below 10th percentile at birth were considered SGA [20,21].

Full-term SGA babies having Ponderal Index (PI) below 2.2 g/cm[3] were treated as asymmetric SGA, and those with Ponderal Index≥2.2 g/cm [3] as symmetric SGA [22–24]. Babies born with multiplegestations, major congenital/ chromosomal/ bodily anomalies atbirth or detected during follow-up and babies with moderate to se-vere illness (meningitis, septicemia, bone or joint infections, necrotiz-ing enterocolitis) and on mechanical ventilation were excluded fromthe study. The written informed consent of one of the parents of eachchild was obtained prior to his / her enrolment in the study on a stan-dardized performa. The study protocol was duly approved by theEthics Committee of the Institute.

Every child was measured for head circumference using standard-ized anthropometric technique [25] with a fiber glass tape up to the ac-curacy of 1 mm at birth, 1 month (time tolerance ±3 days), 3 month,6 month, 9 month and at 12 months of age with a time tolerance limitof ±15 days following a mixed-longitudinal research design in GrowthLaboratory & Growth Clinic of the Child Growth & Anthropology Unit,Department of Pediatrics, PGIMER, Chandigarh. The subjects who didnot report in the hospital for follow-up despite repeated efforts werefollowed and measured in their homes. Age and sex wise distributionof the sample subjects who could be examined during different followups is shown in Table 2.

2.2. Statistical analysis

Age and sex specific average distance (gross size) and velocity growth(rate of growth) related statistics in terms of mean, standard deviation(SD) for head circumference was computed from mixed-longitudinallygathered data on both symmetric and asymmetric SGA and AGA babiesof the two sexes by using analytical method suggested by Tanner(1951) [26]. Student's unpaired t-test was employed to quantify themagnitude of intra-group (Symmetric vs. asymmetric), inter-group(SGA vs. AGA) as well as gender (male vs. female) differences recordedfor distance growth attainments. Mann–Whitney U test was employedto quantify magnitude of these differences for velocity growthattainments.

3. Results

The gestational age wise distribution of both symmetric andasymmetric SGA and AGA subjects of the two sexes is presented inTable (1). Of all the full-term (i.e. 37–40 weeks) symmetric SGA,asymmetric SGA and AGA babies, majority were born at 38 weeks of

Table 1Gestational Age-wise Distribution of Male and Female Symmetric SGA, AsymmetricSGA & AGA Infants.

GestationalAge (Weeks)

SymmetricSGA

AsymmetricSGA

AGA

Male Female Male Female Male Female

37 N 14 8 19 19 9 17% 28.0 16.0 38.0 38.0 18.0 34.0

38 N 19 17 19 11 21 17% 38.0 34.0 38.0 22.0 42.0 34.0

39 N 12 13 7 15 13 9% 24.0 26.0 14.0 30.0 26.0 18.0

40 N 4 12 5 5 7 7% 8.0 24.0 10.0 10.0 14.0 14.0

gestation. However, exception were 38% of asymmetric female SGAbabies who were born at 37 weeks. With advancement of gestationalage, a substantial reduction in the proportion of babies was recorded.As compared to 10% and 14% of the asymmetric and AGA babies ofeach sex, 8% and 24% of male and female symmetric SGA were bornat 40 weeks of gestation.

The mean (SD) birth weight of symmetric SGA male and femalebabies was 2.22 (0.18) kg and 2.25 (0.20) respectively. The correspond-ingfigures formale and female asymmetric SGA babieswere 2.15 (0.23)kg and 2.08 (0.22) kg. The birth weight was 3.00 (0.25) kg for male and2.92 (0.29) kg for female AGA infants. The gender differences for birthweight amongst neither of symmetric and asymmetric SGA as well asAGA infants became statistically significant. There were no differencesof birth weight between male symmetric and asymmetric SGA infantswhile, female symmetric SGA babies weighed significantly (p≤0.001)heavier than their asymmetric peers at birth. At birth both symmetricand asymmetric SGA infants of the two sexes weighed significantly(p≤0.001) lighter than their AGA peers.

A regular increase in the mean head circumference of both typesof SGA and AGA babies was noticed from birth to 12 months of age(Table 2 and Figs. 1 and 2). Head circumference of male asymmetricSGA infants measured significantly larger than their asymmetriccounterparts while, two type of female SGA infants did so between6 and 12 months (Table 2). Head circumference of male asymmetricSGA infants measured significantly larger than female infants. Beingalmost similar in size until 3 months, head circumference amongstsymmetric SGA infants of the two sexes became significantly(p≤0.01) larger in male infants thereafter. Significantly larger headcircumference in male AGA infants than their female peers was noticedat 1(p≤0.05), 9 and 12 (p≤0.01) months. In contrast to their AGAcounterparts, two types and sexes of SGA infants possessed smallermean head circumference throughout infancy. However, exceptionwere male asymmetric SGA and AGA infants at 3 and 6 months whenno difference for head circumference were recorded (Table 2).

The velocity growth curves for head circumference of symmetricSGA, asymmetric SGA and AGA male and female infants showed acontinuous decline depicting maximum rate of growth for head cir-cumference between birth to 1 month and minimum between 9 and12 months of age (Table 3 and Figs. 4 and 5). The differences ingrowth velocity for head circumference between symmetric andasymmetric SGA male infants were statistically non-significant.Though asymmetric SGA female babies possessed higher rate ofgrowth for head circumference than the symmetric SGA infants upto 9 months of age, yet intra-group differences became statisticallysignificant only between 3 and 6 months. While, female symmetricSGA infants possessed statistically significant (p≤0.001) higher rateof growth between 9 and 12 months. Significantly (p≤0.001) higherhead growth velocity in male symmetric SGA infants than female in-fants was recorded up to one month of life. Amongst male asymmetricSGAandAGA infants itmeasuredmore than their female peers between1 and 6 months (p≤0.05) and 6–9 months (p≤0.01) respectively.

Head circumference growthvelocity of both symmetric andasymmet-ric SGA babies of the two sexes measured significantly higher betweenbirth to 1 month of age when contrasted with AGA infants. After that,an inconsistent auxological trend was observed until 9 months. Interest-ingly, between 9 and 12 months of age, a reversal of trend was observedas growth velocity for head circumference measured significantly higherin AGA infants than that recorded amongst two types ofmale SGA and fe-male asymmetric SGA infants (Table 3).

4. Discussion

4.1. Distance growth attainments

The smaller head circumference noticed in symmetric SGA infantsas compared to their asymmetric counterparts has also been reported

Table 2Mean, (SD) and t-values of Head Circumference (cm) of Male and Female Symmetric SGA, Asymmetric SGA and AGA Infants.

Age (months) Symmetric SGA Asymmetric SGA AGA

Male Female Male Female Male Female

N Mean (SD) N Mean (SD) N Mean (SD) N Mean (SD) N Mean (SD) N Mean(SD)

0 50 31.6 (1.01) 50 31.6 (1.02) 50 32.4 (1.11) 50 31.8 (1.04) 50 33.7 (0.80) 50 33.5 (1.25)1 50 35.3 (1.14) 50 34.9 (1.21) 50 35.9 (1.29) 50 35.2 (1.20) 50 36.8 (1.06) 50 36.3 (1.18)3 46 38.3 (1.28) 47 37.9 (0.95) 46 39.4 (1.26) 46 38.2 (1.34) 50 39.7 (1.12) 48 39.3 (1.36)6 44 41.2 (1.33) 48 40.5 (0.93) 46 42.0 (1.12) 42 41.3 (1.08) 47 42.1 (1.27) 47 41.8 (1.09)9 48 42.9 (0.89) 48 42.0 (0.86) 50 43.5 (1.05) 47 42.9 (0.75) 48 44.2 (1.18) 46 43.4 (0.99)12 45 44.0 (1.01) 49 43.4 (1.09) 46 44.5 (1.05) 45 43.8 (0.69) 49 45.7 (1.15) 48 44.8 (1.10)

t-values

Age (months) Gender differences Symmetric SGA VsAsymmetric SGA

Symmetric SGA VsAGA

Asymmetric SGA VsAGA

Symmetric SGA Asymmetric SGA AGA Male Female Male Female Male Female

0 0.020 2.728** 1.210 3.493** 0.727 11.589*** 8.139*** 7.031*** 7.421***1 1.669 2.846** 2.545* 2.634* 1.360 6.984*** 5.722*** 3.800*** 4.371***3 1.894 4.157*** 1.555 4.011*** 1.568 5.568*** 5.847*** 1.234 3.722***6 2.729** 3.224** 1.398 3.182** 3.416** 3.397** 5.932*** 0.262 2.211*9 4.670*** 3.559** 3.604** 3.360** 5.005*** 6.044*** 6.842*** 2.774** 2.617*12 2.939** 3.180** 4.263*** 2.067* 2.353* 7.681*** 6.203*** 5.340*** 4.548***

*p≤0.05, **p≤0.01, ***p≤0.001, df=n-2.

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amongst infants of American [5], Guatemalan [6], Finnish [7], British[8] and Japanese [9] origin. This shows that symmetric SGA babiesdo not make up for auxological loss suffered by them during earlymonths of pregnancy as they postnatally fail to catch-up with theirasymmetric counterparts, in whom head circumference remains al-most unaffected (i.e. spared) during the prenatal period. As a conse-quent to this head circumference in asymmetric SGA infants may begrowing relatively rapidly after birth to yield larger head circumfer-ence. This is clearly evident from upwards shift in head growth curvesfrom being below 3rd centile in asymmetric SGA babies of the twosexes to mid-way between 5-10th centile in male and to reach apoint between 10-25th in female infants. While, it ran around 3rdcentile in male symmetric SGA infants and between 5-10th centileof 2000 CDC growth charts [27] in female infants (Fig. 3). From therelatively better position of head growth curve in female symmetricand asymmetric SGA infants than their male counterparts, it willnot be out of place to infer that female babies appear to have morepotential for catch-up growth than their male peers. Similar trendhas also been noticed amongst AGA infants representing presentstudy in whom head circumference growth curve ran between 10

Fig. 1. Comparison of Head Circumference (cm) of Male Symmetric SGA, AsymmetricSGA, AGA and Normal Infants.

and 25th centile in case of male and between 25-50th percentile ofCDC growth charts in female infants. Fitzhardinge & Steven (1972)[28] reported that mean growth curve for head circumference reached10th–25th centile by 6 months of age in which these infants continuedto grow until 6 years of age. Babson (1970) [29] also reported a steadyupward shift so that by 1 year mean head circumference was onlyabout 1 SD below the mean having been about 2 SD below the meanat birth. Davies (1980) [30] also noticed pronounced upward shift ofhead growth in light-for-date babies indicating that the growth of thebrain is considerably hindered by intra-uterine influences for whichthey might be making up during postnatal life.

The smaller mean head circumference noticed in SGA as comparedto their AGA as well as affluent Indian [31], normal Punjabi [32] &MGRS [33] counterparts during first year of life corroborate with thefindings of Babson (1970) [29], who reported that significant disparityin head size of full-term but severely underweight for gestational ageinfants from the normal sized infant at birth, was only partly reducedby the end of first year as is the case in the current study subjects.

A substantial degree of growth retardation amongst SGA infants(without categorizing into symmetric and asymmetric) having

Fig. 2. Comparison of Head Circumference (cm) of Female Symmetric SGA, AsymmetricSGA, AGA and Normal Infants.

Table 3Mean, (SD), and z-values of Head Circumference Growth Velocity of Male and Female Symmetric SGA, Asymmetric SGA and AGA Infants.

Age Interval (months) Symmetric SGA Asymmetric SGA AGA

Male Female Male Female Male Female

Mean (SD) Mean (SD) Mean (SD) Mean (SD) Mean (SD) Mean (SD)

Birth-1 3.64 (0.71) 3.24 (0.99) 3.54 (0.89) 3.42 (0.84) 3.08 (1.02) 2.76 (1.04)1–3 3.05 (0.86) 3.01 (0.64) 3.49 (0.90) 3.03 (0.54) 2.85 (0.78) 3.05 (0.90)3–6 2.78 (0.79) 2.64 (0.75) 2.65 (0.72) 3.04 (0.81) 2.44 (0.72) 2.45 (0.76)6–9 1.72 (0.78) 1.53 (0.39) 1.63 (0.74) 1.64 (0.61) 1.95 (0.66) 1.57 (0.54)9–12 1.12 (0.41) 1.33 (0.53) 1.05 (0.43) 0.95 (0.37) 1.56 (0.66) 1.36 (0.43)

z-values

Age Interval (months) Gender differences Symmetric SGA VsAsymmetric SGA

Symmetric SGA VsAGA

Asymmetric SGA VsAGA

Symmetric Asymmetric AGA Male Female Male Female Male Female

Birth-1 2.530** 0.556 1.435 0.463 1.391 3.316** 2.143* 2.808** 3.422***1–3 0.504 2.337* 0.858 1.833 0.150 1.201 0.034 3.414*** 0.1023–6 0.498 2.022* 0.348 0.558 2.142* 1.928* 1.690 1.358 3.685***6–9 0.293 0.555 2.508** 0.274 1.027 1.735 1.187 2.168* 0.2709–12 1.806 1.128 1.223 0.728 3.570*** 3.739*** 1.080 3.926*** 4.201***

*p≤0.05, **p≤0.01, ***p≤0.001, df=n-2. Velocity: birth to 1 month (cm/ month), 1 to 3 month (cm/ 2 month), 3 to 6, 6 to 9 and 9 to 12 (cm/3 month).

476 H. Kaur et al. / Early Human Development 88 (2012) 473–478

smaller head circumference, in comparison to their normal weightpeers have also been reported in India [34-37] as well as in otherparts of the world [38-42]. Srivastava et al. (1978) [34] related thispattern of growth amongst their small-for-date babies to a higher fre-quency and duration of illness than the control group. Khatua et al.(1987) [35] argued that the handicaps of the small-for-date infantsbesides being related to the severity and duration of intra-uterinegrowth retardation may be partly due to their genetically determinedgrowth pattern, postnatal environment and nutrition. Dobbing(1981) [43] suggested that some of the regulations of catch-up

Fig. 3. Comparison of Head Circumference (cm) of Male and Female Sy

might reside in the brain and undernutrition which is enforced duringthe period of maximum brain growth result in a failure to completelyrecover the growth deficit.

However, our observations are at variance with the findings ofVohr & Oh (1983) [44] who reported that head circumference mea-surements in SGA infants were found to be comparable to their AGAcounterparts by 1 year of age, and was considered as a favorablesign for subsequent development in SGA infants. No significant differ-ences in mean head circumference of AGA and severe intrauterinegrowth retarded (SIUGR) babies between birth to 12 months was

mmetric SGA, Asymmetric SGA and AGA Infants with CDC Charts.

΅ Velocity: birth to 1 month (cm/ month), 1 to 3 month (cm/ 2 month), 3 to 6, 6 to 9 & 9 to 12 (cm/ 3 month)

Fig. 4. Comparison of Head Circumference Growth Velocity of Male Symmetric SGA, Asymmetric SGA, AGA and Normal Infants.

477H. Kaur et al. / Early Human Development 88 (2012) 473–478

observed by Bhargava et al. (1976) [45]. Similarly, the concept ofadaptive head sparing in SIUGR babies at birth (larger heads as com-pared to non-growth retarded infants of similar birth weight) wasreported by Kramer et al. (1989) [46]. Watt [39] also reported thatSGA infants were more likely to exhibit head sparing at birth(pb0.02) than their matched controls.

4.2. Growth velocity

The pattern of continuous decline from birth to 12 months of agedemonstrated by velocity growth curves plotted for head circumferenceof symmetric, asymmetric SGA and AGA infants (Figs. 4 and 5) is similarto that observed amongst normal Swedish [47], MGRS [33] and Delhi[48] infants. The higher rate of head circumference growth observedamongst asymmetric SGA female infants than their symmetric SGAcounterparts until 9 months of age is similar to that recorded for lowponderal index (asymmetric) as compared to short-for-date (symmet-ric) infants during infancy byHolmes et al. (1977) [5]. The higher rate ofgrowth for head circumference amongst wasted (asymmetric) than thenon-wasted (symmetric) infants reported by Davies et al. (1979) [49]corroborates with our findings. This shows that in contrast to symmet-ric SGA infants, asymmetric SGA infants have more potential to growrapidly and this may be due to influence of head sparing effect experi-enced by them during prenatal life and appears to be a valid reasonfor larger head circumference possessed by asymmetric SGA infants ascompared to symmetric ones.

The results of higher rate of growth observed amongst male SFDinfants as compared to their female counterparts studied in Allahabad[34] during first 6 months of life and America [38] from birth to 1 yearof age corroborates with the findings of present study where malesymmetric and asymmetric SGA as well as AGA infants possessed

Fig. 5. Comparison of Head Circumference Growth Velocity of Female Symmetric SGA,Asymmetric SGA, AGA and Normal Infants.

higher growth velocity for head circumference than their femalecounterparts. While, normal male infants studied by Karlberg et al.(1968) [47] and MGRS [33] possessed higher rate of growth forhead circumference than female ones until 6 months thereafter, itmeasured similar amongst infants of both the genders.

Both types of SGA infants possessed higher rate of growth for headcircumference as compared to their AGA peers during first half of in-fancy. This shows that SGA infants try to undo the effect of nutritionalinsult experienced by them during fetal period by growing rapidlythan their normal counterparts and try to come at par with thempostnatally. Significantly (pb0.001) higher rate of growth recordedfor head circumference of term SGA infants of Finnish origin [7]than their control infants during first three months of life, and a com-parable auxological trend during remaining period of infancy corrob-orates with velocity growth pattern encountered amongst our infants.The findings of Srivastava et al. (1978) [34] are also in completeagreement with the results of present study as their SGA infants pos-sessed greater rate of growth for head circumference than their full-term normal control infants during first 6 months of life. Babson[29] also documented higher rate of growth for head circumferencein term under-grown infants than normal sized infants and attributedthis trend to the influence of “preferential” head growth which oc-curred in-utero in these infants. Similar results amongst SFD infantsof American origin have also been presented by Cruise [34]. Infer-ences drawn by Bhargava et al. (1970) [50] for full-term SGA infantsare also similar to our findings where our both symmetric and asym-metric SGA infants of the two sexes exhibited higher rate of growththan the AGA infants till 6 months of age. Thereafter, their term SGAinfants continued to possess higher growth velocity for head circum-ference than the controls which is contrary to pattern of growthexhibited by our SGA infants. Similar rate of growth amongst SIUGRand AGA infants observed in another study by Bhargava et al.(1976) [45] during first year of life remains at variance with the find-ings of present study. The observation of Khatua et al. (1987) [35] arealso in disagreement with our findings as they noticed exactly similarrate of growth amongst their SGA and term control infants duringsecond half of infancy. However, at present no clear explanationcould be offered to reason out this different velocity growth relatedtrend noticed amongst Indian infants except for its attribution totheir different ethnic origins. The other possibility may relate to thefact that SGA is multifactorial. Depending on the etiology, durationof insult and genetic reasons the growth potential of SGA infantsmay be variable.

Conflict of interest statement

None declared.

478 H. Kaur et al. / Early Human Development 88 (2012) 473–478

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