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Study of Parents and Children (ALSPAC)

WHAT’S KNOWN ON THIS SUBJECT: In a previous study, it was found that most excess weight gain in English children had taken place by age 5. The authors suggested that interventions to prevent obesity should focus only on children younger than 5 years of age.

WHAT THIS STUDY ADDS: From birth to 5 years of age was not characterized by the greatest excess weight gain in a larger sample of English children and adolescents. Greatest gains in weight and BMIzscores occurred during mid-childhood. Efforts to prevent obesity should not only focus on preschool children, but also include school-aged children and adolescents.

abstract

OBJECTIVES:To test the hypothesis that most excess weight gain oc-curs by school entry in a large sample of English children, and to determine when the greatest gain in excess weight occurred between birth and 15 years.

METHODS:Longitudinal data were collected annually from birth to 15 years in 625 children. Weight and BMI at each time point were ex-pressed relative to UK 1990 growth reference as z scores. Excess weight gain was calculated as the group increase in weight and BMIz

scores between specific time periods.

RESULTS:Weightzscore did not increase from birth to 5 years (mean difference: 0.04 [95% confidence interval (CI):⫺0.03– 0.12]P⫽.30) but increased from 5 to 9 years (mean difference: 0.19 [95% CI: 0.14 – 0.23]

P⬍.001). BMIzscore increased from 7 to 9 years (mean difference: 0.22 [95% CI: 0.18 – 0.26]P⬍.001), with no evidence of a large increase before 7 years and after 9 years.

CONCLUSIONS:Our results do not support the hypothesis that most excess weight gain occurs in early childhood in contemporary English children. Excess weight gain was substantial in mid-childhood, with more gradual increases in early childhood and adolescence, which indicates that interventions to prevent excess weight should focus on school-aged children and adolescents as well as the preschool years.

Pediatrics2011;127:e730–e736

AUTHORS:Adrienne R. Hughes, PhD,aAndrea Sherriff,

PhD,bDebbie A. Lawlor, PhD,cAndrew R. Ness, PhD,dand

John J. Reilly, PhDe

aDepartment of Sports Studies, University of Stirling, Stirling, Scotland;bDental School, University of Glasgow, Glasgow, Scotland;cMRC Centre for Causal Analyses in Translational Epidemiology, School of Social and Community Medicine, Oakfield House, Bristol, England;dDepartment of Oral and Dental Science, University of Bristol, Bristol, England; andeUniversity of Glasgow Medical Faculty, Division of Developmental Medicine, Yorkhill Hospitals, Glasgow, Scotland

KEY WORDS

ALSPAC, obesity, overweight, children, adolescents

ABBREVIATIONS

ALSPAC—Avon Longitudinal Study of Parents and Children CiF—Children in Focus

This publication is the work of the authors. Dr Hughes and Prof Reilly will serve as guarantors for the contents of this article.

www.pediatrics.org/cgi/doi/10.1542/peds.2010-0959

doi:10.1542/peds.2010-0959

Accepted for publication Nov 22, 2010

Address correspondence to John J. Reilly, PhD, School of Psychological Sciences and Health, University of Strathclyde, Jordanhill Campus, 76 Southbrae Dr, Glasgow G13 1PP, Scotland. E-mail: john.j.reilly@strath.ac.uk

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2011 by the American Academy of Pediatrics

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There has been a rapid rise in the prev-alence of childhood obesity in recent years in the United Kingdom1and more

widely,2,3although in some nations

pe-diatric obesity prevalence seems to be stabilizing.4,5 Obesity is now 1 of the

most common pediatric health prob-lems, and it has a range of adverse ef-fects on physical and psychosocial health in childhood and adulthood.6,7

There is increasing evidence that growth in early life may be important to later risk of obesity, and excessive weight gain in early childhood in par-ticular seems to be strongly predictive of later obesity risk.8,9 Timing of the

“adiposity rebound” during the pre-school years has long been considered to be a potential critical period for pro-gramming of later obesity, but evi-dence for programming is inconclu-sive,10 and early childhood may be

important to later obesity risk simply because that is when “obesogenic” lifestyles and growth trajectories are often established.11 An improved

un-derstanding of the natural history of obesity development (how and when obesity typically develops) would im-prove our understanding of the etiol-ogy of pediatric obesity, and so inform the development of future interven-tions aimed at obesity prevention.12,13

However, it is unclear at present when excess weight gain typically occurs in childhood (eg, early, mid-, or late child-hood) and therefore when best to tar-get obesity prevention interventions.

In a recent study, Gardner et al14

exam-ined excess weight gain (defined as an increase in weight z score) between birth, 5 years, and 9 years in small co-hort of 233 English children. Gardner et al14found that weight gain was

sub-stantial from birth to 5 years, whereas subsequent weight gain from 5 to 9 years was much smaller. Therefore, the study indicates that the preschool period is critical to the development of excess weight gain in English children.

This study has received a great deal of attention in the United Kingdom be-cause its findings have important im-plications for public health policy, indi-cating that future pediatric obesity prevention strategies should target preschool children if obesity is set by school age.14 However, the study by

Gardner et al14included only 134 boys

and 99 girls who were followed to 9 years and used change in weight z

score as the sole measure of weight status. Given the importance of these findings, the hypothesis that excess weight gain develops largely before the age of school entry needs to be fur-ther explored, ideally in a larger sam-ple of children followed for a longer period, and extended by the inclusion of a more specific measure of weight status such as BMIzscore. Therefore, the primary aim of the present study was to test the hypothesis (suggested by Gardner et al14) that most excess

weight gain occurs by 5 years in a larger sample of English children, by comparing changes in weight and BMI

zscore between birth and 15 years. A secondary aim was to determine when the greatest gain in excess weight occurred.

METHODS

The Avon Longitudinal Study of Parents and Children (ALSPAC) is a large pro-spective cohort study of children born in the Southwest of England in 1991 and 1992; study design and methods are de-scribed in detail elsewhere.15,16 Briefly,

14 541 pregnant women with an ex-pected date of delivery between April 1991 and December 1992 were enrolled, resulting in 13 988 children alive at 1 year. Detailed information has been col-lected by using questionnaires, data ex-traction from medical notes, linkage to routine information systems, and at re-search clinics for children.

A 10% sample of the ALSPAC cohort, known as the Children in Focus (CiF)

group, attended research clinics at 4, 8, 12, 18, 25, 31, 37, 43, 49, and 61 months, when detailed physical exam-inations were undertaken. The CiF group was chosen at random from the last 6 months of ALSPAC births (1432 families attended at least 1 clinic). The CiF group was broadly socioeconomi-cally representative of both the entire ALSPAC cohort15and the United

King-dom. From age 7 onward, the entire ALSPAC cohort was invited to attend regular research clinics. Ethical ap-proval for the study was obtained from the ALSPAC Law and Ethics Committee and the local health service research ethics committees. In the present study, data from the CiF group are used as a means of replicating the findings of Gardner et al14and meeting

our primary aim. Data from the CiF sample were available for children up to 15 years old, and so were also used to meet our secondary aim of explor-ing when the greatest increases in weight status occurred during child-hood and adolescence.

Study Procedures

Gestational age and birth weight as re-corded in the delivery room was ob-tained from medical charts, and birth length was measured by trained ALSPAC staff within 24 hours of birth where possible. At each measurement occasion, length/height was measured to 0.1 cm, and weight was measured to 0.1 kg in underwear. BMI was calcu-lated as weight (kg)/length (m)2 at

each time point. Weight and BMI at each time point were converted to z

scores by comparison with British 1990 reference data17by using age at

measurement for each individual (or gestational age for birth weight z

score).

Testing the ‘Gardner Hypothesis’

The present study aimed first to repli-cate the study by Gardner et al14 by

quantifying gain in weight z score in

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school by 5 years old): Gardner et al14

considered weightzscore changes be-fore 5 years, and from 5 to 9 years. Although a degree of “regression to the mean” in weight status is to be ex-pected in individuals,17the pattern of

group changes in weight status in United Kingdom cohorts studied after the onset of the obesity epidemic in the late 1980s has been 1 of increases in weight status (eg, BMI z score) with age and over time.14,18,19 Support for

the Gardner hypothesis would be pro-vided in the present study by evidence of increases in mean or median weight

zscore (or BMIz score), which were most marked up to around the age of school entry (age 5 in the United King-dom), and which were relatively stable or declining thereafter. The present study would be inconsistent with the Gardner hypothesis if the increases in weightzscores (and/or BMIzscores) were more substantial after school en-try (eg, between ages 5 and 9 years) than before age of school entry.

To meet our secondary aim (to identify periods of greatest gains in weight sta-tus across a wider age range than studied by Gardner et al14) we

con-ducted a formal comparison of gains in weight and BMIzscores across the period of birth to 15 years.

Increases in weight and BMI z score with age are to be expected in United Kingdom cohorts of children and ado-lescents born in the 1990s,14,18,19 and

these are considered as excess weight gain because they represent greater gains in weight status than expected from UK 1990 reference data.14,17

In the present study, changes in weight status during specific time periods

was calculated (using the same

method as Gardner et al14) as the

dif-ference in weight z score and BMI z

score between ages (eg, weight gain at

BMI z score would reflect excess weight gain, as defined by Gardner et al14

In the present study, we used the CiF group in the analyses because re-search clinic weight and height mea-surements were available in early childhood (ie, up to 5 years) for this sample, and so this provided the best opportunity to replicate the findings of Gardner et al, and to examine our sec-ond aim of assessing when excess weight was greatest between infancy and age 15. Children born preterm (ie, ⬍37 weeks’ gestation; n⫽40) were excluded from the analysis.

Research clinic-assessed weight and height data for the entire ALSPAC co-hort were only available at birth and from 7 years onward. Although the CiF sample was selected randomly from the entire cohort, and would not be ex-pected to be biased by selection, we checked this by comparing patterns of excess weight gain in the entire cohort and the CiF sample from 7 years old.

Statistical Analysis and Power

Power was fixed by the size of the CiF group, and so no formal power calcu-lation was conducted. However, the sample size in the present study was much larger than the sample used by Gardner et al,14by which the

hypothe-sis being tested was suggested. Statis-tical analyses were performed using SPSS 16.0 (SPSS Inc, Chicago, IL). Weight and BMIzscores were normally distributed, and data are presented as means (SD).

To meet our primary aim of testing the Gardner hypothesis, within-child changes in weight z score and BMI z

score during specific time periods (eg, birth to 5 years and 1 to 5 years versus 5 to 9 years) were calculated. The results obtained were then compared with

and BMIzscore was determined using pairedttests. Changes between speci-fied time points and 95% confidence in-tervals for the changes are presented along withPvalues. The analytical ap-proach was identical to that taken by Gardner et al,14although in the present

study, changes in both BMIzscore and weightzscore were available, whereas Gardner et al reported only weight z

scores.

To meet our secondary aim, to extend our exploration of the timing of in-creases in weight and BMIzscores be-yond the age of 9, when Gardner et al14

stopped reporting data, within-child changes were calculated up to 15 years old, and the significance of changes between specified periods again was assessed by use of pairedt

tests and 95% confidence intervals for the changes.

We reran all analyses, taking the follow-ing considerations into account: includ-ing children born at⬍37 weeks’ gesta-tion; restricting analysis to participants with all data at all time periods (n

447); and restricting analysis to partici-pants with a difference of 1.5 to 2.5 years between measurement periods. Similar results were obtained for the rerun anal-yses (available from author on request). We compared study participants who were included in the analyses of change in weightzscore from 1 to 3 years and from 11 to 13 years with those who were included in the 1- to 3-year analysis but were lost to follow-up by the 11 to 13 years analysis for a number of charac-teristics usingttests.

RESULTS

Characteristics of Study Participants

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ⱕ37 weeks. Of the 1358 (730 boys, 628 girls), 96.3% were from the majority (white) ethnic group (1297); 773 (59.6%) mothers had been educated to 16 years old, and 525 (40.4%) had been educated to 18 years or beyond; 7.0% (85) of mothers and 87 (9.3%) of their partners were obese (defined as BMI ⬎30.0, with self-reported weights at 12 weeks’ gestation).

We compared study participants who were included in the analyses of change in weightzscore from 1 to 3 years and from 11 to 13 years with those who were included in the 1- to 3-year analysis but were lost to follow-up by the 11- to 13-year analysis. Compared with those who were in-cluded in both analyses, slightly more boys were lost to follow-up and had mothers who were slightly less edu-cated and were more likely to be obese (Supplemental Table 4 includes com-parisons of those followed up versus lost to follow-up;Supplemental Table 5 includes anthropometric characteris-tics from birth to 15 years). Weight and BMI z scores were similar between those followed up and lost to follow-up.

Primary Aim: Test of the ‘Gardner Hypothesis’; Changes in Weightz Score to 5 Years and 5 to 9 Years Described Longitudinally

Weight and BMI z scores for the CiF sample are included in Table 1 from birth to 15 years old (n⫽625 at age 15). In Table 1 it is shown that, in con-trast to the predictions from Gardner et al, mean BMI and weight z scores increased steadily over the study pe-riod, and changes seem most marked after the age of school entry.

The changes in weightzscores from birth to 5 years and 5 to 9 years are shown in Table 2, in the most direct comparison with the Gardner et al study.14 In contrast to the findings of

Gardner et al, weightz score did not increase significantly from birth to 5

years, whereas increase in weight z

score was statistically significant from 5 to 9 years in the present study (Table 2). Findings were similar in both boys and girls; weight z score did not change significantly from birth to 5 years (zscore for boys was 0.06,P

.21; for girls it was 0.02,P⫽.78) and increased significantly from 5 to 9 years among boys (zscore: 0.26,P

.001) and to a lesser extent in girls (z

score: 0.10,P⬍.001).

Primary Aim: Test of the ‘Gardner Hypothesis’; Changes in BMIz Score From 1 to 5 Years and 5 to 9 Years Described Longitudinally

There were small but statistically sig-nificant increases in BMIzscore from 1 to 5 years and 5 to 9 years (Table 2), although-in contrast to the prediction of Gardner et al- there were no marked differences in BMI z score gain be-tween the 2 time periods. Among boys, BMIzscore increased from 1 to 5 years (0.10zscore,P⫽.01) and 5 to 9 years (0.14z score,P⬍.001). Among girls, there was an increase in BMIzscore from 1 to 5 years (0.09zscore,P⫽.03) but not from 5 to 9 years (-0.03zscore,

P⫽.46).

Secondary Aim: Timing of Excess Weight and BMI Gain to 15 Years; Changes in Weight and BMIz Scores Described Longitudinally

The change in weight and BMIzscores to 15 years old are shown in Table 3. Weightzscore did not increase signif-icantly in early childhood (ie, 1–7 years). In contrast, there were statisti-cally significant gains in weightzscore from 7 to 9 years and 9 to 11 years, with no marked increases thereafter. BMI z score increased significantly from 7 to 9 years, with no evidence of a large increase before 7 or after 9 years of age.

Results obtained from the entire ALSPAC cohort (from age 7 to 15) did

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not differ substantively from those ob-tained in the CiF sample

(Supplemen-tal Table 6andSupplemental Table 7).

DISCUSSION

Main Findings

Modest gains in weight and BMI z

scores were evident throughout the period of the present study, although these were generally most marked, and most likely to be statistically sig-nificant in the periods after the age of school entry, in particular between 7 to 9 years. Moreover, within-child cor-relations between BMIzscores across childhood in the present study were significant, but declined with age: for example, correlation coefficients from age 3 were 0.80 at age 5, and fell to 0.49

at age 11, which suggests more move-ment in weight status than might be predicted from the findings of Gardner et al.14Thus, the present study does not

support the hypothesis suggested in the study by Gardner et al14that most

excess weight gain occurs in early childhood (before school entry) in En-glish children, or that weight status is set by the time of school entry.

Gardner et al14quantified changes in

weightzscore only, and from birth to 9 years. In the present study we investi-gated changes in both weight and BMI

zscores in a larger sample of children over a longer period of time, from birth to 15 years. The reasons for the differ-ences in findings of the present study and those of Gardner et al are unclear.

3-year difference means that a period effect might have been operating: the extent to which children of any age were susceptible to excess weight gain might have differed between periods. Geographical or socioeconomic differ-ences between the 2 populations might also contribute to differences between our study findings and those of Gardner et al14

In the present study we used the CiF subgroup of the ALSPAC cohort for the analyses because weight and height measurements were available in early childhood (ie, up to 5 years) for this sample, whereas data were only avail-able at birth and from 7 years onward in the entire ALSPAC cohort. However, to examine the consistency of our find-ings across the entire cohort, we also examined excess weight gain from birth to 7 years and from 7 to 15 years in the entire ALSPAC cohort, and the results confirmed the findings from the CiF group (seeSupplemental Table

6andSupplemental Table 7).

Study Implications and

Comparisons With Other Studies

One interpretation of the study by Gard-ner et al,14which has gained widespread

currency in the United Kingdom,20is that

if most excess weight gain occurs before school entry, then obesity prevention in-terventions should focus on preschool children, with a reduced emphasis on such interventions during later child-hood and adolescence.20 Because the

results of the present study are not consistent with those of Gardner et al14 the present study provides no

support for the suggestion that obe-sity prevention and treatment strat-egies should be focused exclusively on young children.

Evidence from other populations should be considered when

examin-Change (SD) Interval

Weightzscore, age group (y),n

0–5, 932 0.04 (1.18) ⫺0.03–0.12

5–9, 760 0.19 (0.57) 0.14–0.23

BMIzscore, age group (y),n

1–5, 883 0.10 (0.84) 0.04–0.15

5–9, 757 0.06 (0.75) 0.01–0.12

Because the mean age of the sample who attended the 9-year-old clinic was 9.8 years, the change in weightzscore from 5 to 8 years (mean age: 8.6 y) also was calculated; similar results were obtained for the CiF group combined and for boys and girls separately.

TABLE 3 Changes in Weight and BMIzScores to Age 15 Years

Mean Change (SD)

95% Confidence Interval

Weightzscore, age group (y),n

1–3, 969 ⫺0.02 (0.65) ⫺0.06–0.02

3–5, 867 0.009 (0.46) ⫺0.02, 0.04

5–7, 801 0.02 (0.41) ⫺0.003–0.05

7–9, 803 0.16 (0.39) 0.14–0.19a

9–11, 766 0.15 (0.36) 0.12–0.18a

11–13, 672 0.001 (0.44) ⫺0.03–0.03

13–15, 562 ⫺0.05 (0.43) ⫺0.09–⫺0.02b

BMIzscore, age group (y),n

1–3, 954 0.10 (0.78) 0.06, 0.15a

3–5, 854 ⫺0.01 (0.59) ⫺0.05, 0.03

5–7, 798 ⫺0.14 (0.55) ⫺0.18–⫺0.10a

7–9, 803 0.22 (0.54) 0.18–0.26a

9–11, 766 0.04 (0.45) 0.01–0.08b

11–13, 672 ⫺0.02 (0.49) ⫺0.06–0.01

13–15, 562 0.04 (0.47) 0.005–0.08c

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ing the Gardner hypothesis. In some studies the age-related pattern of obesity prevalence does not suggest that the years before school entry are especially obesogenic relative to later periods. It is suggested by re-cent data from the United States, for example, that obesity risk increases with age from the preschool years into the middle and elementary

school years.21In their review,

Whit-lock et al22 also suggested that

screening for child and adolescent obesity would not identify those likely to be obese as adults very ef-fectively, implying that weight status is not “set” by school entry.

Identifying the optimal time to target pediatric obesity preventive and treat-ment interventions will depend on a number of factors, including studies of

the natural history of excess weight gain,12,13but also the efficacy and

cost-effectiveness of interventions applied at different ages.23,24

Direct comparisons of the findings of the present study with previous stud-ies is difficult because so few previ-ous studies have focused on quanti-fying the extent and timing of excess weight gain in contemporary chil-dren and adolescents, with the

nota-ble exception of the study by Gardner et al. However, it was reported in a recent study of a large sample of En-glish adolescents25 that persistent

obesity was generally established before 11 years, and marked in-creases in obesity risk were not present in ages 11 to 15 in England, broadly consistent with the findings of the present study.

Strengths and Limitations of the Present Study

A degree of attrition in longitudinal studies is inevitable, and although some characteristics of participants lost to follow-up differed slightly from those retained in later analyses, changes in both weight and BMI z

scores were similar between groups in the present study; it seems likely that loss to follow-up did not have a marked impact on study findings. Anal-yses restricted only to those children with complete follow-up data were es-sentially the same as those with the entire sample.

One major issue arising from the present study is generalizability. The characteristics of the ALSPAC study participants will have a bearing on generalizability. The sample was broadly representative of the United Kingdom in terms of socioeconomic status, but estimated maternal obesity prevalence seems to be low because it is based on self-reported weights ob-tained at 12 weeks’ gestation in 1991 and 1992. Both the present study and the study by Gardner et al14that we

attempted to replicate were very de-pendent on the UK 1990 reference data for weight and BMI. Apparent patterns in timing of excess weight gain may have arisen because of features inher-ent to the reference population, and both the present study and that of Gardner et al are limited by any weak-nesses in the reference data. Extrapo-lation of the present study findings to other populations and other sets of population reference data should also be considered with caution: differ-ences between populations and

be-tween reference data sets mean that the magnitude and pattern of change in weight and BMI z score might be quite different in other cohorts in other settings. The present study is best considered as an exploration of the pattern and timing of excess weight gain within the English popula-tion of children and adolescents.

CONCLUSIONS

Our results do not support the hypoth-esis that most excess weight gain oc-curs in early childhood in contempo-rary English children. In this cohort born in the early 1990s and followed to 2008, excess weight gain was substan-tial in mid-childhood, with more grad-ual increases in early childhood and adolescence. Population-based inter-ventions to prevent excess weight should therefore focus on school-aged children and adolescents as well as the preschool years.

ACKNOWLEDGMENTS

The United Kingdom Medical Research Council (Grant 74882), the Wellcome Trust (Grant 076467), and the Univer-sity of Bristol provide core support for ALSPAC. The United Kingdom Medical Research Council (G0600705) and the University of Bristol provide core fund-ing for the MRC Centre of Causal Anal-yses in Translational Epidemiology.

We thank the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interview-ers, computer and laboratory techni-cians, clerical workers, research scien-tists, volunteers, managers, receptionists, and nurses.

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DOI: 10.1542/peds.2010-0959 originally published online February 21, 2011;

2011;127;e730

Pediatrics

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Adrienne R. Hughes, Andrea Sherriff, Debbie A. Lawlor, Andrew R. Ness and John J.

Children (ALSPAC)

Timing of Excess Weight Gain in the Avon Longitudinal Study of Parents and

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located on the World Wide Web at:

The online version of this article, along with updated information and services, is

http://pediatrics.aappublications.org/content/suppl/2011/02/11/peds.2010-0959.DC1 Data Supplement at:

by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.

Figure

TABLE 2 Tests of the Gardner Hypothesis: Changes in Weight z Score and BMI z Score from 0 to 5and 5 to 9 Years of Age

References

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