Factors Associated With Early Adiposity Rebound

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Factors Associated With Early Adiposity Rebound

Ahmad R. Dorosty, BSc, MSc*; Pauline M. Emmett, BSc, SRD‡; Imogen S. Cowin, BSc‡;

John J. Reilly, BSc, PhD*; and the ALSPAC Study Team

ABSTRACT. Objective. The age at which body mass index (BMI) increases after its nadir in childhood, adi-posity rebound (AR), is a critical period for the develop-ment of obesity. Children with early AR are at substan-tially increased risk of adult obesity. Few studies have examined the factors that influence the timing of the AR. The aims of this study were to test for influences on the timing of the AR, and to test the hypothesis that early AR is promoted by high-protein intake.

Design and Participants. Longitudinal cohort study of 889 children representative of the United Kingdom, followed from birth to 5 years.

Main Outcome Measures. We tested for differences in dietary intake, parental BMI, socioeconomic status, and childhood BMI between 3 groups of children character-ized by the following: very early AR (at or before 43 months), early AR (from 49 but before 61 months), and later AR (after 61 months).

Results. There was no evidence of associations be-tween dietary protein intake, or any other dietary vari-able, and timing of the AR. Children with very early AR and early AR had parents with significantly higher BMI, and were significantly more likely to have at least 1 obese parent.

Conclusion. This study does not support the hypoth-esis that early AR is promoted by high-protein intake. None of the dietary variables tested were significantly associated with timing of the AR, and timing of AR was not associated with socioeconomic status. Parental obe-sity was associated with an earlier AR. Pediatrics 2000; 105:1115–1118;obesity, child, body mass index, macronu-trients, adiposity rebound.

ABBREVIATIONS. AR, adiposity rebound; BMI, body mass index; ALSPAC, Avon Longitudinal Study of Pregnancy and Childhood; UK, United Kingdom; SDS, standard deviation score; ANOVA, analysis of variance.

T

here is now considerable evidence that

adipos-ity rebound (AR), the point at which the body

mass index (BMI) increases after its nadir in

childhood, is a critical period for the development of

obesity.

1

_{An early AR (younger age at onset of AR) is}

associated with higher BMI in adolescence and

young adulthood,

2– 4

_{and substantially increased risk}

of adult obesity, as defined by BMI.

5

At present, the factors that influence the timing of

the AR are unclear, and research aimed at identifying

these is indicated.

5

_{An understanding of which}

fac-tors influence the timing of AR might facilitate

obe-sity prevention, and might also identify important

mechanisms of energy balance regulation. In a small

study of French children (n

⫽

112) higher protein

intake at age 2 years was associated with earlier AR,

6

and it was suggested that the association was causal.

The primary aim of the present study was to test this

hypothesis using a larger sample of children. A

sec-ondary aim was to assess the influence of a number

of other factors on timing of the AR in a large-scale

prospective cohort study, the Avon Longitudinal

Study of Pregnancy and Childhood (ALSPAC

7

_).

METHODS Subjects

ALSPAC is a prospective cohort study of the determinants of health during childhood in the Bristol-Avon area of the United King-dom (UK).7_{The cohort has been described in detail elsewhere}7,8_and

is broadly representative of the UK population in terms of socioeco-nomic status, although with a slight underrepresentation of ethnic minority families, and slight overrepresentation of wealthier fami-lies.8_{Summary anthropometric measurements of the cohort from}

infancy and early childhood did not differ significantly from UK reference data,9_{and in fact were almost identical to these data.}8

Subjects used in the analyses for the present study represented a 10% subsample of the cohort, randomly selected for more detailed inves-tigations. These children (n⫽889) were born in 1991 and 1992 and are representative of the entire cohort.7,8_{Measurements on this}

sub-sample were made at frequent intervals: birth, 4, 8, 12, 18, 24, 31, 37, 43, 49, and 61 months.

Childhood Measurements

Height, Weight, BMI, and AR

At each measurement occasion up to 24 months, length was measured to 0.1 cm using the Harpenden Neonatometer and Holtain Kiddimetre (Holtain, Dyfed, Wales). From 24 months height was measured to 0.1 cm using the Leicester Height Measure (Cranlea, Birmingham, United Kingdom). Weight was measured to 0.1 kg at each measurement occasion in underwear using SECA scales (SECA Ltd, London, United Kingdom). BMI was then cal-culated for each measurement period.

Timing of AR was assessed, as a categorical variable, by visual inspection, using the method previously described.2,3_{This involved}

identifying an upward trend in BMI after its nadir. To identify that such a trend had occurred (and to distinguish it from random fluc-tuation and measurement error) it was necessary to: 1) specify that all consecutive measurements of BMI after the nadir showed an in-crease, and 2) require that any increase in BMI after the nadir had to equal or exceed 0.1 kg/m2_{. In fact, changes in BMI between}

measure-ments of such a small magnitude around the time of AR were rare, but this additional criterion was included to reduce any subjectivity in the assessment and to avoid basing judgements on changes in BMI which were within the limits of measurement error. This definition of rebound was therefore slightly more conservative than the defini-tions in the literature on which it was based.2,3_{We established that}

our definition was the same as that of the literature method on which

From the *University of Glasgow Department of Human Nutrition, Yorkhill Hospitals, Glasgow, Scotland; and the ‡Unit of Paediatric and Perinatal Epidemiology, Institute of Child Health, University of Bristol, Bristol, United Kingdom.

Received for publication Apr 6, 1999; accepted Sep 8, 1999.

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it was based by consulting the principal author of the original report2

and conferring over the BMI versus age plot for 9 children who comprised a wide range in timing of AR. This procedure confirmed that our methods for assessing the timing of AR produced the same conclusions.

The BMI was expressed as a standard deviation score (SDS), also known as theZscore, relative to contemporary UK reference data9_{(Child Growth Foundation Software, London, UK).}

Dietary and Nutrient Intake

Dietary intake data were obtained in all children by 3-day prospectively collected household measures records at ages 8 and 18 months. To replicate the earlier study6 _{presentation of the}

analysis is confined here to the dietary data at 18 months, al-though conclusions did not differ when dietary data were ana-lyzed at the other time period. From these records we calculated absolute intake of energy and macronutrients, energy intake per kg body mass, and macronutrient intake as a percentage of dietary energy intake using the most recent computerized version of McCance and Widdowson’sThe Composition of Foods(Royal Soci-ety of Chemistry, Cambridge, UK).

Parental Information

Parental heights (to 1 cm) and weights (to 0.5 kg, pregravid weight of mothers) were obtained by self-report.7_{Socioeconomic}

status (social class category) was determined in the standard way10

from the occupation of the mother’s partner. Educational attain-ment of the mother was obtained by self-report and summarized in 5 categories from lowest (category A) to highest (category E). These 5 categories were as follows: A, Statutory school attendance to age 16 years, with no formal qualifications attained; B, Attain-ment of technical or vocational qualifications by age 16 years; C, Attainment of at least 1 pass in academic examinations taken at age 16; D, Attainment of academic examinations taken at age 18; and E, Attainment of university degree.

Statistical Analysis

The aim of the analysis was to test for differences between chil-dren with earlier AR and the rest, using timing of the AR as a categorical variable. Very early AR was defined here as at or before 43 months; early AR from 49 but before 61 months; and later AR after 61 months. Although these definitions were somewhat arbitrary, we confirmed that our results were not a function of the precise catego-ries chosen by repeating the analyses with different combinations of categories to represent different timing of AR. Differences between categories distinguished based on continuous variables were tested for significance using 1-way analysis of variance (ANOVA) with follow-up multiple comparisons incorporating Bonferroni correc-tions as appropriate. Differences for categorical variables were tested for significance using␹2_tests.

RESULTS

Dietary and Nutrient Intake at 18 Months of Age

Dietary and nutrient intakes at age 18 months,

avail-able for 772 of the 889 subjects, are given in relation to

timing of the AR in Tables 1 (absolute intakes) and 2

(relative intakes). There was no evidence of differences

in dietary intake associated with timing of the AR.

There was no evidence of any association between

protein intake and timing of the AR.

Childhood BMI

There was no evidence of differences in absolute

BMI between those with very early or early AR and

the rest at any age before 4 years (ie, before the

rebound). There was some evidence that girls with

very early rebound had higher BMI SDS before the

rebound than the rest. After the rebound had

oc-curred BMI SDS and absolute BMI were significantly

higher in those children who had rebounded very

early (1-way ANOVA;

P

⬍

.001; Fig 1).

Parental BMI

Mean BMI of parents was significantly higher in

those children with very early rebound (Table 3).

Having at least 1 obese parent (defined as BMI

ⱖ

30.0) was also significantly associated with both

very early and early AR.

Parental Education and Socioeconomic Status

There was no evidence of any associations

be-tween parental educational attainment or

socioeco-nomic status, and timing of the AR (Table 3).

DISCUSSION

There is currently considerable interest in critical

periods for obesity development

1

_{because these}

might offer opportunities for obesity prevention, and

a way of understanding the mechanisms by which

energy balance is regulated. Although the AR

con-stitutes only 1 of 3 such critical periods,

1

_{the timing of}

the AR does have a significant influence on BMI in

adolescence and adulthood, and risk of adult obesity

as defined by BMI.

2–5

_{Rolland-Cachera et al}

6

_found

that an early AR was associated with high-protein

intake, and speculated that this relationship was

causal.

11

_{This was based on a relatively small study}

(112 subjects) and the authors concluded that their

findings should be confirmed by other studies. To

our knowledge, the present study is the only attempt

to replicate that of Rolland-Cachera et al.

6

_The

TABLE 1. Absolute Dietary and Nutrient Intake at 18 Months in Relation to Timing of AR, Mean (SD)

Absolute Intake n Protein (g/d) Fat (g/d) Carbohydrate (g/d) Energy (KJ/kg/d) Energy (KJ/d)

Boys

Very early 25 43.7 (9.5) 50.2 (10.9) 145.5 (34.1) 422.0 (105.5) 5059 (999)

Early 85 42.4 (10.0) 48.7 (10.2) 142.5 (23.9) 418.7 (71.2) 4932 (749)

Later 322 42.3 (10.4) 47.6 (11.9) 140.0 (28.8) 417.8 (85.0) 4845 (928)

Total 432 42.4 (10.2) 47.9 (11.5) 140.8 (28.2) 417.8 (83.7) 4874 (900)

Girls

Very early 28 40.0 (9.2) 43.6 (10.2) 138.6 (29.5) 407.4 (76.6) 4633 (811)

Early 71 40.1 (9.7) 45.1 (10.8) 128.5 (28.1) 418.3 (77.9) 4526 (807)

Later 241 39.8 (9.9) 45.5 (12.5) 131.0 (24.4) 414.9 (95.0) 4575 (995)

Total 340 39.9 (9.8) 45.3 (11.9) 131.1 (29.1) 414.9 (90.0) 4569 (943)

Total

Very early 53 41.7 (9.5) 46.7 (11.0) 141.9 (31.6) 414.1 (90.4) 4834 (921)

Early 156 41.3 (9.9) 47.1 (10.6) 136.2 (26.7) 418.7 (74.1) 4747 (800)

Later 563 41.2 (10.2) 46.7 (12.2) 136.2 (29.4) 416.6 (89.6) 4729 (966)

Total 772 41.3 (10.1) 46.8 (11.8) 136.5 (29.0) 416.6 (86.7) 4740 (931)

No differences reached statistical significance.

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present study was a large-scale, prospective test of

the hypothesis that higher protein intake promotes

earlier AR. We found no evidence to support this

hypothesis, although group mean values for the

per-centage of energy from protein (Table 2) were not

quite as high as those of the children who

experi-enced early AR in the Rolland-Cachera study.

6

_In

fact, there was no clear evidence that any of the

dietary variables were related to timing of the AR

(Tables 1 and 2). This result, like the others reported

in the present study, was independent of the

catego-ries chosen to represent differences in timing of the

AR: our conclusions were not altered when different

combinations of categories were chosen to represent

differences in timing of the AR.

A number of possible mechanisms of early AR

have been proposed. These include parental control

over feeding in early childhood, which can be

coun-terproductive and lead to impaired ability to regulate

energy intake.

12

_{Although we did not test this}

hy-pothesis directly, there was no evidence of any

asso-ciation between energy intake and timing of the AR

in this study. It has been suggested that early AR

might be associated with gestational diabetes,

13

_and

might be a marker for early maturation

1,14

_{but we did}

not measure these variables. Our evidence of no

association between socioeconomic status and timing

of the AR is consistent with one recent European

study

15

_{and is potentially important given current}

concerns over the interrelationships between

socio-economic status and obesity.

There were significant associations between

paren-tal BMI, parenparen-tal obesity (defined as BMI

ⱖ

30.0), and

earlier AR (Table 3), and, indeed, these were the only

variables we tested that were positively and

signifi-cantly associated with earlier AR. This observation

provides further emphasis that the child of obese

parents could be a useful target for obesity

preven-tion efforts. However, it should be noted that

paren-tal BMI was less confidently measured than the other

variables because it was based on self-report.

Self-reports of height, and to a greater extent weight, are

subject to small but significant biases.

16

_{It is also}

worth noting that the effect of timing of AR on risk of

adult obesity is independent of parental obesity.

5

The present study was considerably larger than

previous investigations of the causes/correlates of

early AR. Children who had very early AR in our

study were present in relatively large numbers,

and they experienced AR around 2 years earlier

than mean values from studies in the literature

(mean values of AR typically 5–7 years;

2–5

_{). This}

might, in part, reflect a secular trend to earlier AR

9

_:

previous studies were conducted on cohorts that

experienced AR

⬎

20 to 30 years ago;

2–5

_{our cohort}

experienced AR in the mid-1990s and AR occurs

earlier now than in the past.

9

_{Therefore, it seems}

likely that children in our category of very early

AR were unusual at least in the sense that their AR

occurred early relative to that of their peers, but

even in this group there was little evidence of

differences in the variables measured, with the

exception of parental obesity. It is conceivable that

genetic factors might be important in influencing

timing of the AR,

1

_{but the relative importance of}

genotype and environment on the AR remain

un-clear.

5

_{The secular trend to earlier AR}

9

_suggests

that there are strong environmental influences on

the timing of the AR.

CONCLUSION

In summary, the present study suggests that dietary

energy and macronutrient intakes are not associated

with timing of the AR. In particular, there was no

evidence that higher protein intake was associated with

early AR. Timing of AR was not associated with

socio-economic status. The only factor significantly

associ-ated with timing of the AR in the present study was

parental BMI. Children of parents with high BMI, or

with at least 1 obese parent, were significantly more

likely to have an earlier AR. Parental obesity is a

well-established risk factor for obesity

17

_{and the present}

study suggests that it may operate, at least in part, via

an influence on the timing of the AR. In the absence of

any other markers of early AR, the factors currently

known to be associated with obesity risk, including age

and parental obesity,

16

_{inactivity/watching television,}

18

and preschool activity

19

_{should continue to be used as}

the principal targets of obesity prevention measures in

children.

TABLE 2. Macronutrient Intake as Percentage of Dietary En-ergy Intake at 18 Months in Relation to Timing of AR, Mean (SD)

Relative Intakes n Protein Fat Carbohydrate

Boys

Very early 25 14.5 (2.2) 37.4 (3.6) 48.1 (5.0) Early 85 14.4 (2.4) 37.1 (4.2) 48.6 (5.2) Later 322 14.6 (2.2) 36.8 (4.9) 48.6 (5.7) Total 432 14.6 (2.2) 36.9 (4.6) 48.5 (5.6) Girls

Very early 28 14.4 (1.7) 35.4 (5.8) 50.2 (6.3) Early 71 14.8 (2.3) 37.5 (5.5) 47.6 (6.4) Later 241 14.6 (2.2) 37.2 (4.4) 48.2 (5.2) Total 340 14.6 (2.2) 37.1 (4.8) 48.2 (5.6) Total

Very early 53 14.5 (1.9) 36.3 (4.9) 49.2 (5.8) Early 156 14.6 (2.4) 37.3 (4.8) 48.1 (5.8) Later 563 14.6 (2.2) 37.0 (4.7) 48.4 (5.5) Total 772 14.6 (2.2) 37.0 (4.7) 48.4 (5.6)

No differences reached statistical significance.

Fig 1. Mean BMI SDS (Zscore) in children characterized by very

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ACKNOWLEDGMENTS

ALSPAC was supported by the Wellcome Trust, Department of Health, Ministry of Agriculture Fisheries and Food, Medical Re-search Council, British Gas, and other companies.

Ahmad Dorosty was supported by the Iranian Ministry of Health and Medical Education.

We thank all of the parents and children who took part in the study, and the ALSPAC Study Team, which consists of inter-viewers, technicians, clerical workers, scientists, volunteers, and managers.

In addition, we thank Dr Marie Francoise Rolland-Cachera for her help and advice on the methodology for defining timing of the AR. We also thank Dr Jan Love of the Robertson Center for Biostatistics for statistical advice, and the Child Growth Foundation, London, for providing the growth monitoring equipment.

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resource for assessing the magnitude of long term effects of prenatal and perinatal events.Contemp Rev Obstet Gynecol.1996;8:89 –91 8. ALSPAC. Children of the nineties. Available at: http://alspac2.

ich.bris.ac.uk/ALSPACext

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development of adiposity from 1 month of age to adulthood.Ann Hum Biol.1987;14:219 –229

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TABLE 3. Parental Characteristics in Relation to Timing of AR

Groups Very Early AR Early AR Later AR Total

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

Paternal BMI

Boys 23 25.8 (3.4) 77 25.4 (3.6) 260 25.2 (3.1) 360 25.2 (3.2)

Girls 27 26.3 (4.2)* 65 24.9 (3.1) 218 25.1 (3.3) 310 25.2 (3.3)

Total 50 26.1 (3.8)* 142 25.2 (3.4) 478 25.1 (3.2) 670 25.2 (3.3)

Maternal BMI

Boys 26 25.3 (4.4)**¤ ₈₇ _{23.8 (4.0)} ₃₃₈ _{23.0 (3.5)} ₄₅₁ _{23.2 (3.7)}

Girls 31 24.0 (3.7) 82 23.6 (5.0) 263 23.3 (4.1) 376 23.4 (4.3)

Total 57 24.6 (4.1)** 169 23.7 (4.5) 601 23.1 (3.8) 827 23.3 (4.0)

n (%) n (%) n (%) n (%)

Percentage with 1 obese parent

Boys 7/27 (25.9)** 17/89 (19.1)† 29/350 (8.3)† 53/466 (11.4)

Girls 7/33 (21.2) 11/82 (13.4) 36/274 (13.1) 54/389 (13.9)

Total 14/60 (23.3)** 28/171 (16.4)† 65/624 (10.4)† 107/855 (12.5)

Maternal education category A–C

Boys 17/28 (60.7) 50/90 (55.6) 193/356 (54.2) 260/474 (54.8)

Girls 18/34 (52.9) 54/83 (65.1) 159/280 (56.8) 231/397 (58.2)

Total 35/62 (56.4) 104/173 (60.1) 352/636 (55.3) 491/871 (56.4)

D,E

Boys 11/28 (39.3) 40/90 (44.4) 163/356 (45.8) 214/474 (45.1)

Girls 16/34 (47.1) 29/83 (34.9) 121/280 (43.2) 166/397 (41.8)

Total 27/62 (43.5) 69/173 (39.9) 284/636 (44.6) 380/871 (43.6)

Socioeconomic status I and II

Boys 10/22 (45.4) 28/76 (36.8) 118/282 (41.8) 156/380 (41.1)

Girls 9/27 (33.3) 18/73 (24.6) 85/231 (36.8) 112/331 (33.8)

Total 19/49 (38.8) 46/149 (30.9) 203/513 (39.6) 268/711 (37.7)

III to V

Boys 0/22 (0.0) 5/76 (6.6) 17/282 (6.0) 22/380 (5.8)

Girls 3/27 (11.1) 9/73 (12.3) 31/231 (13.4) 43/331 (13.0)

Total 3/49 (6.1) 14/149 (9.4) 48/513 (9.4) 65/711 (9.1)

Significant differences between very early AR group and the rest at *P⬍.05, **P⬍.01. † Significant difference between later AR group and early AR group,P⬍.05.

Parental obesity defined as BMIⱖ30.0.

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DOI: 10.1542/peds.105.5.1115

2000;105;1115

Pediatrics

the ALSPAC Study Team

Ahmad R. Dorosty, Pauline M. Emmett, SRD?; Imogen S. Cowin, John J. Reilly and