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International Journal of Obesity (2006) 30, S11S17

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ORIGINAL ARTICLE
Early adiposity rebound: causes and consequences for
obesity in children and adults
MF Rolland-Cachera, M Deheeger, M Maillot, F Bellisle

Research Unit on Nutritional Epidemiology INSERM U557/INRA U1125/CNAM/PARIS 13, Human Nutrition Research
Center of Ile de France, Bobigny, France

Childhood obesity is an important public health problem, with a rapidly increasing frequency worldwide. Identification of critical
periods for the development of childhood and adolescent obesity could be very useful for targeting prevention measures.
Weight status in early childhood is a poor predictor of adult adiposity status, and most obese adults were not obese as children.
We first proposed to use the body mass index (BMI) charts to monitor individual BMI development. The adiposity rebound (AR)
corresponds to the second rise in BMI curve that occurs between ages 5 and 7 years. It is not as direct a measure as BMI at any
age, but because it involves the examination of several points during growth, and because it is identified at a time when
adiposity level clearly change directions, this method provides information that can help us understand individual changes and
the development of health risks. An early AR is associated with an increased risk of overweight. It is inversely associated with
bone age, and reflects accelerated growth. The early AR recorded in most obese subjects and the striking difference in the mean
age at AR between obese subjects (3 years) and non-obese subjects (6 years) suggest that factors have operated very early in life.
The typical pattern associated with an early AR is a low BMI followed by increased BMI level after the rebound. This pattern is
recorded in children of recent generations as compared to those of previous generations. This is owing to the trend of a steeper
increase of height as compared to weight in the first years of life. This typical BMI pattern (low, followed by high body fatness
level) is associated with metabolic diseases such as diabetes and coronary heart diseases. Low body fatness before the AR
suggests that an energy deficit had occurred at an early stage of growth. It can be attributable to the high-protein, low-fat diet
fed to infants at a time of high energy needs, the former triggering height velocity and the latter decreasing the energy density
of the diet and then reducing energy intake. The high-fat, low-protein content of human milk may contribute to its beneficial
effects on growth processes. Early (pre- and postnatal) life is a critical period during which environmental factors may
programme adaptive mechanisms that will persist in adulthood. Under-nutrition in fetal life or during the first years after birth
may programme a thrifty metabolism that will exert adverse effects later in life, especially if the growing child is exposed to
overnutrition. These observations stress the importance of an adequate nutritional status in childhood and the necessity to
provide nutritional intakes adapted to nutritional needs at various stages of growth. Because the AR reflects particular BMI
patterns, it is a useful tool for the paediatrician to monitor the childs adiposity development and for researchers to investigate
the different developmental patterns leading to overweight. It contributes to the understanding of chronic disease
programming and suggests new approaches to obesity prevention.
International Journal of Obesity (2006) 30, S11S17. doi:10.1038/sj.ijo.0803514

Keywords: adiposity rebound; growth; child nutrition; trends; metabolic diseases

Introduction occurring in early life could play a major role.1,2 Identifica-


tion of early markers of adult body adiposity is useful for
Although obesity, particularly childhood obesity, is increa- clinicians to monitor the child fatness development and for
sing worldwide, no decisive evidence emerges to account researchers to investigate the origin of obesity. Childhood
for this trend. Factors such as nutrition in childhood and weight status is a poor predictor of adult adiposity and most
adulthood provide an inconclusive explanation for adult obese adults were not obese as children.3 Other anthropo-
health outcomes. By contrast, it seems that risk factors metric parameters must be investigated. Age at adiposity
rebound (AR), recorded on individual BMI growth curves,
has been identified as an indicator predicting adult fatness.4
Correspondence: Dr MF Rolland-Cachera, UMR 557 INSERM/U1125 INRA/
This indicator may help identify the critical periods of
CNAM/Paris 13, SMBH Universite Paris 13, 74 rue Marcel Cachin-93017,
Bobigny cedex, France. adiposity development and the determinants of future
E-mail: mf.cachera@smbh.univ-paris13.fr obesity and health risks.
Early adiposity rebound
MF Rolland-Cachera et al
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Assessment of the age at adiposity rebound
Weight(kg)/Height2 (m)
31
Nutritional status during growth is currently assessed on the Overweight area Case 1
basis of weight and height. Weight for age and weight for 29 Girls
height are recommended for young children by the World
Health Organization.5 However, the first indicator ignores 27
97th
height and the second ignores age. Weight-for-height indices
according to age include the three parameters (weight, 25
Case 3 90th
height and age) simultaneously. As it is highly correlated
23
with weight and body fat, and weakly related to stature, the 75th

weight/(height)2, Quetelet or body mass index (BMI) has


21 50th
been selected to predict adiposity in children.6 In the early
1980s, the first BMI distribution reference charts,6 revised 10 Case 2 25th
19
years later,7 were constructed for all ages throughout child-
hood (Figure 1) and adulthood.7 This method is now used 17
10th

worldwide. Case 4 3th


The development of the BMI during growth parallels the 15
development of more direct measures of body adiposity such
as skin folds. On the average, a rapid increase of the BMI 13
occurs during the first year of life. The BMI subsequently
declines and reaches a minimum around the age of 6 years, 11
before beginning a sustained increase up to the end of Underweight area
growth. The point of minimal BMI value (the nadir of the 9
Age, years
BMI curve) is the start of the AR.4,8
Different methods are used to assess age at AR. It was first 0 1 3 5 7 9 11 13 15 17 19 21
assessed by visual inspection.4,8 This involves identifying an 6
Figure 1 BMI reference centiles for French girls. Four example of BMI
upward trend in the BMI after the nadir. In some cases, the development plotted against the reference charts case no. 1, fat child at 1
year, remained fat after an early adiposity rebound (2 years); case no. 2, fat
descending phase of BMI is followed by a plateau. In this
child at 1 year, did not stay fat after a late adiposity rebound (8 years); case no.
case, the age at AR corresponds to the start of the steep BMI 3, lean child at 1 year, became fat after an early adiposity rebound (4.5 years);
increase (e.g. 8 years in case 4; Figure 1). In order to identify case no. 4, lean child at 1 year, remained lean after a late adiposity rebound
the upward trend in BMI, Dorosty et al.9 specified that all (8 years) (after Rolland-Cachera et al.8).
consecutive measurements of the BMI after the nadir should
show an increase, and required that any increase in the BMI
after the nadir had to equal or exceed 0.1 kg/m2. Gasser the childs BMI predicts adult fatness only poorly. Case 3 in
et al.10 determined the AR from the velocity curve of the Figure 1 (a thin child at 4 years becoming overweight after an
BMI. Age at AR corresponded to the point where the velocity early AR) points out that many cases of overweight that are
curve became positive after a fall of BMI in infancy and early diagnosed at adolescence actually have their origin much
childhood. Polynomial models to describe the patterns of earlier in life. The BMI chart can be a very useful tool for the
change in BMI are also used.1115 Age at minimum BMI is paediatrician to monitor the BMI development in children.
derived from these models. Comparing different approaches, Several studies have investigated the association between
a recent study15 concluded that estimating AR visually the age at AR and adult adiposity.1114,1618 Using the French
appears to best reflect the physiological basis of the AR. sample6,19 of the International Growth Study,20 we estab-
Using this method, mean age at AR in the French reference lished that age at AR was significantly associated with BMI
population was 6.271.6 years.4,8 This is similar to the level at later ages:4 the earlier the AR, the higher the BMI or
generally reported mean values, varying between 5 and 7 the subscapular skin fold at age 21 years.8 Regression analysis
years according to the population studied and the method performed on this sample indicated that each year decrease
used.1116 in age at AR was associated with a 0.84 kg/m2 (0.82 in boys
and 0.85 in girls) increase in the predicted BMI level at age 21
years (Po0.001) (unpublished data). In a study conducted in
the US, each year decrease in age at AR was associated with a
Prediction of adult fatness 2.5 kg/m2 increase in the predicted BMI level at age 1923
years.17
AR and adult fatness Whether an early AR reflects increased fat or lean body
On average, AR takes place by the age of 6 years, but in mass was questioned.21 A study following children between
individual cases, as shown in Figure 1, it may occur earlier or 5 and 9 years found that differences in BMI during the AR
later.8 These individual BMI patterns explain why, before AR, period were caused specifically by alteration in body fat

International Journal of Obesity


Early adiposity rebound
MF Rolland-Cachera et al
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assessed by dual X-ray absorptiometry (DXA) rather than by a 19
alteration in lean mass. Children undergoing early AR gained
fat at a faster rate than children who rebounded at a later 18
age.22 From this observation, it is justified to go on using the
term Adiposity rebound4 rather than using BMI rebound 17
as proposed later on.17
We also investigated the association between AR and bone

BMI (Kg/m2)
16
age: an early AR was associated with advanced skeletal
maturity.4 This association, also reported by Williams et al.,13
15
is consistent with the association between rapid growth and
later high BMI2326 and, as a rule, with the accelerated
14
growth of all body tissues observed in obese children.27
Accelerated growth is often reported in low birth weight
infants.23 Using the data of the French reference study,19 no 13

association was recorded between the age at AR and birth


BMI 6y Low High
weight (r 0.08; P 0.23) (unpublished data). An early AR 12
0 2 4 6 8 10
then reflects rapid post-natal growth, rather than catch up
AGE (years)
growth following low birth weight. In a study conducted in
New Zealand, AR arose earlier in children who were tall at b 19
3 years, and an early AR was associated with early menarche,
suggesting that the timing of rebound is an indicator of
18
physical maturity.28

17
BMI (Kg/m2)

Comparison between indicators predicting adult adiposity


It has been suggested that an early AR predicts later fatness 16
because it identifies children whose BMI is high21,29 and/or
crossing centiles upwards.29 BMI at the time of AR (57 years)
15
and BMI centile crossing were proposed as more direct
indicators than AR for predicting later fatness.3,10,13,17,21,29
Actually, different aspects must be considered. 14
A high BMI level at the age of 6 years is significantly
associated with later high BMI, but also with previous high 13
Adiposity rebound Early Late
BMI levels. In the Zurich study,10 the correlation between 0 2 4 6 8 10
BMI at 6 years and adult BMI was 0.60. It was of the same AGE (years)
magnitude (r 0.66) between the BMI at 6 years and the BMI Figure 2 Comparison between two indicators predicting adiposity deve-
at 1 year. Using the data of the French longitudinal study of lopment. Two subgroups are constituted on the basis of the median of the
nutrition and growth (ELANCE) described earlier,30,31 we distribution of each indicator converted into Z-scores: BMI at the age of 6
have compared the BMI patterns according to either BMI at 6 years (a) and age at AR (b) (n 104).

years or age at AR (Figure 2). Figure 2a shows that a high BMI


at the age of 6 years is associated with high BMIs at all ages,
starting from birth. By contrast, an early AR is associated mechanisms by which body fat is acquired seem to be at least
with a high BMI at adult age, but with normal or even low as important as the consequences of excess fat per se in the
BMI level before the rebound (Figure 2b). The association pathogenesis of diabetes, hypertension and cardiovascular
between an early AR and low or average BMI before the AR diseases.35
was reported in various studies.8,9,12,28 Consequently, as a Consequently, as compared with a high BMI at 6 years or
rule, a child fat at age 6 years is more likely to be always fat, with centile crossing,29 the early AR, which is associated with
whereas a child with an early AR is more likely to have a a particular BMI trajectory, has different implications and is
normal or even low adiposity level in early life and to likely associated with different environmental factors.
develop fatness only from the time of AR. The BMI trajectory
of subjects who were thin in infancy and thereafter put on
weight rapidly (Figure 2b) is associated with insulin resis- BMI pattern in the obese
tance and coronary heart diseases.3234 In a study conducted Mean age at AR in the obese generally occurs around the age
in India,33 despite an increase in BMI between the ages of 2 of 3 years compared to 6 years in reference populations. In a
and 12 years, none of the subjects with impaired glucose study conducted in 62 obese children examined in a
tolerance or diabetes were obese at the age of 12 years. The department of paediatric endocrinology, mean age at AR

International Journal of Obesity


Early adiposity rebound
MF Rolland-Cachera et al
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was 3.2 years.8 None of these children had an AR later than 1

the age of 6 years. Two children had their AR at the age of 0.8
Height
6 years (i.e. average) and more than half of them (55%) had
Weight
an AR at, or before, the age of 3 years.8 These observations, 0.6
Born in 1985
together with similar data reported elsewhere16,36 showing

Z-score
0.4
that most obese subjects displayed an early AR, are in BMI
0.2
contrast to the observation that most obese adults were not Reference population
(born in 1955)
obese as children. An early AR is a better indicator of the 0
0 2 4 6 8 10 12 14 16 18 20
timing of the origin of obesity than a high BMI, which may
-0.2
only appear after a progressive increase over many years.37,38
Age, years
The very early AR recorded in most obese subjects suggests -0.4

that factors promoting obesity have operated very early in Figure 3 Trajectories of growth in two longitudinal studies carried out 30
life and probably several years before the AR. This observa- years apart: mean Z-scores for height, weight and BMI in children born in
tion is consistent with studies showing that early (pre- and 1985,31 compared to a mean value of zero for children of the French reference
population, born in 1955.19
post-natal) life is a critical period for later risks.1,2

trajectory during childhood is associated with insulin


resistance and coronary vascular diseases in later life.3234
Secular trends in growth patterns Similar secular trends are reported in other countries.
Anthropometric measurements recorded in a longitudinal
Childhood obesity is increasing but other growth parameters study conducted in German children from 197842 were
are also changing. Secular trends to increasing adult height, compared with more recent data recorded from 2001.43 At
weight and BMI have been clearly documented. At birth, the age of 2 years, BMI was lower in the second study
weight trends are small.39 In childhood, height trends tend (Po0.034), which was due to a gain of height as compared to
to be greater than in adulthood, owing to the associated the earlier study. In England, height increased in different
advance in maturation. The increase in height from one age groups between 1972 and 1994, weight for height also
generation to the next occurs mainly in the first 2 years of showed a slight decline in the youngest (5- or 6-year-old)
life. The adult height trend matches that at age 2 years, so children, it remained unchanged in the 7- and 8-year- old
that the increment in adult height has already been achieved and showed an increase in the 9- and 10-year- old.44
by age 2 years.39 Similar trends are observed in France40
where two 20-year follow-up studies were conducted under
similar conditions 30 years apart.19,31 Weight, height and
BMI of subjects born in 1985 (ELANCE study) were converted Factors associated with an early AR and increased
into Z-scores for each age and sex, in relation to the fatness
population born in 1955 as the reference, using the LMS
method41 (Figure 3). At the end of growth, subjects born in Positive energy balance results from high energy intake or
1985 are taller, heavier and fatter31 than those born in low physical activity. Results of a longitudinal study showed
1955.19 Over the 30 years period, subscapular skin fold an increased fatness development in children with a seden-
thickness at adult age increased from 8.8 to 14.2 mm in tary lifestyle. This increase appeared after an early AR.45
males and from 9.9 to 17.3 mm in females. Height trend is Nutritional studies have investigated the influence of early
maximum between 4 and 10 years and decreases until nutrition on either later fatness development or on the age at
adulthood. As reported earlier,39 the adult height trend is AR. The association between nutritional intakes at the age
about the same as the trend at age 2 years. The decreased of 2 years and fatness development was investigated in
height trend observed from the age of 10 years is accounted our longitudinal study of nutrition and growth.30 Both high
for by the earlier growth cessation in children born in 1985, protein (% energy) and high energy intakes were associated
owing to their advanced maturation.31 At the age of 20 years, with increased BMI at 8 years, but following different BMI
BMI is higher in the recent study, but this trend appears from patterns. BMI values in subjects consuming a high-energy
the age at AR only. Before the AR, BMI was lower in children diet at 2 years were high at all ages with average age at AR.
born in 1985, with a maximum trend at age 2 years. The BMI values in subjects consuming a high-protein diet tended
lower BMI in early life can be explained by the greater gain in to be lower in early ages and became higher after an early
height as compared to weight. Mean age at AR occurred at AR occurred. The BMI pattern of subjects consuming a high-
6.2 years in children born in 1955 and at 5.6 years in those energy diet is similar to the pattern in subjects with a high
born in 1985. As compared to subjects born in 1955, the BMI level at 6 years (Figure 2a), whereas the BMI pattern
growth pattern of subjects born 30 years later typically shows of subjects consuming a high-protein diet is similar to the
a rapid height gain and a low BMI in early life, followed pattern in subjects with an early AR (Figure 2b). No
by an early AR and subsequent high fatness.31 This BMI association was found between the percentage of energy

International Journal of Obesity


Early adiposity rebound
MF Rolland-Cachera et al
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from the other nutrients (fat and carbohydrates) and age at level followed by high BMI after the AR) can be the
AR or fatness level at 8 years. Other studies found an consequence of reduced energy balance owing to high-
association between high protein intake in infancy and later protein, low-fat intake in early life followed by increasing fat
high fatness,24,46 whereas others did not.9,47 A study intake with age. In the recent years, most studies report that
conducted in Danish children found an association with infants have been fed a diet with a higher proportion of
measures of body size (weight and height) but not with body energy coming from protein and lower intakes of fat than
fat.48 would have been the case in the past.6165 These changes
We previously proposed that the characteristics of child- could account for the secular trends of accelerated linear
hood obesity, that is, increased stature and body mass (lean growth and decreased BMI in the first 2 years of life as shown
and fat)27 were the consequence of high protein intakes in Figure 3. Decreased fat intake in French children was
inducing changes in hormonal status.49,50 High plasma mainly owing to a decreased consumption of whole milk,
insulin like growth factor-1 (IGF1) concentrations and compensated for by low-fat milk and dairy products.64 The
reduced growth hormone (GH) secretion (spontaneous or daily consumption of whole milk in 2-year-old children was
in response to a wide variety of stimuli) are characteristic 206 g in 1973 and 90 g in 1986, whereas the consumption
features of children with simple obesity.51 Increased IGF1 of low-fat milk (half skimmed and skimmed milk) was 44 g
could promote hyperplasia in all tissues, including adipose in 1973 and 216 g in 1986. The decline in energy intake
tissue, and decreased GH levels could decrease lipolysis, in infants and children over the last decades is very likely the
promoting the development and maintenance of large fat consequence of the low-energy protein-rich diet they
stores. A study conducted in 2.5-year-old Danish children currently consumed.50
found that animal protein (from milk but not from meat or Undernutrition at any time in early life (during fetal life as
vegetables) was positively associated with serum IGF-1 reflected by low birth weight1 or before an early adiposity
concentrations and height.52 rebound3234) may predispose to later risks. A relative energy
Our results regarding the association between nutritional deficit66 may programme thrifty metabolism and mechan-
intakes in infancy and growth patterns have underlined the isms of adaptative thermogenesis.35 Lucas67 proposed the
inadequate nutrient balance of the infant diet in industria- term programming for the process in which the program-
lized countries.50 By the age of 1 year, the infant diet is ming stimulus exerts long-term effects when applied at a
characterized by high intake of protein (B4 g/kg body critical or sensitive period. Adaptation to low fat intake in
weight or 16% of total energy) and low intake of fat early life may have adverse effects when, later in life,
(B28%). Protein intake represents about 34 times the children will eat a more abundant high-fat diet. The low-
protein needs. The nutrient imbalance is remarkable con-
sidering that human milk provides 6% of energy as proteins
and 52% as fat.53 The protective effect of human milk 60

reported in some studies could be explained by its low


protein and high fat content. Breast-fed infants have a slower
growth.23 A similar observation was recorded in our long- 50
itudinal study described earlier.30 Length increase between
birth and 2 years was 36.872.8 cm in breast-fed infants and
38.172.9 in those who were not breast fed (P 0.03)
40
(unpublished data). There is now increasing evidence that
a rapid growth (weight and/or length) in infancy or early
childhood can predispose to later risks.26 It is associated with
% Energy

large subsequent weight gain17,23,24,54 and a central body fat 30 % Protein


pattern23,25 and also with a risk of diabetes,55 cardiovascular % Fat
disease56 and cancer.57,58 % CHO
Paradoxically, the proportion of fat in the infant diet is low
20
at a period of high energy needs. Subsequently, the
percentage of energy provided by fat increases. In our
longitudinal study of nutrition and growth,59,60 the percen-
tage of fat intake increased from the age of 10 months to 6 10
years (27.4 at 10 months, 32.6 at 2 years, 36.5 at 4 years and
37.3 at 6 years), then plateaued until 16 years and reached
38% at 20 years (Figure 4), whereas it should be high in early 0
infancy and should then gradually decrease during the first 0 5 10 15 20
years of life.53 Age, years
Similar fat intake patterns were reported in other coun- Figure 4 Nutrient intake (percentage of energy) changes by age in subjects
tries.53 The BMI pattern associated with an early AR (low BMI followed longitudinally from early childhood to adulthood.59,60

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MF Rolland-Cachera et al
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fat diet given to infants may result from strategies to prevent 7 Rolland-Cachera MF, Cole TJ, Sempe M, Tichet J, Rossignol C,
obesity or cardiovascular diseases in industrialized countries, Charraud A. Body mass index variations: centiles from birth to 87
years. Eur J Clin Nutr 1991; 45: 1321.
despite general agreement that dietary fat content should
8 Rolland-Cachera MF, Deheeger M, Avons P, Guilloud-Bataille M,
not be reduced in early life,53,68 and from poor living Patois E, Sempe M. Tracking adiposity patterns from 1 month to
conditions in the developing world. adulthood. Ann Hum Biol 1987; 14: 219222.
9 Dorosty AR, Emmett PM, Cowin IS, Reilly JJ, the ALSPAC Study
team. Factors associated with early adiposity rebound. Pediatrics
2000; 105: 11151118.
Conclusion 10 Gasser TH, Ziegler P, Seifert B, Molinari L, Lardo R, Prader A.
Prediction of adult skinfolds and body mass from infancy
through adolescence. Ann Hum Biol 1995; 22: 217233.
In order to prevent obesity, it is of great interest to identify 11 Siervogel RM, Roche AF, Guo S, Mukherjee D, Chumlea WC.
subjects at risk before adiposity reaches high levels. Age at AR Patterns of change in weight/stature2 from 2 to 18 years:
predicts later fatness, but because it involves the examina- findings from long-term serial data for children in the Fels
longitudinal growth study. Int J Obes Relat Metab Disord 1991; 15:
tion of several points during growth, the AR mainly reflects
479485.
the growth pattern rather than absolute fatness level. 12 Whitaker R, Pepe MS, Wright JA, Seidel KD, Dietz WH. Early
Considering the age at AR allows a clear understanding of adiposity rebound and the risk of adult obesity. Pediatrics 1998;
changing BMI pattern in individuals. The early AR recorded 101: e5.
13 Williams S, Davie G, Lam F. Predicting BMI in young adults from
in most obese subjects suggests that determinants of obesity childhood data using two approaches to modelling adiposity
have operated early in life. An early AR is associated with rebound. Int J Obes Relat Metab Disord 1999; 23: 348354.
low fatness before the rebound and high fatness after the 14 Guo SS, Huang C, Maynard LM, Demerath E, Towne B, Chumlea
rebound. Similar BMI patterns are observed in relation with WC et al. Body mass index during childhood, adolescence and
young adulthood in relation to adult overweight and adiposity:
various other situations (secular trends, sedentary life style, the fels longitudinal study. Int J Obes Relat Metab Disord 2000; 24:
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