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Differences in the mean fat cell diameter of males between 1 and 48 months of age.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOI.OGY 65.341-945 (19811
Differences in the Mean Fat Cell Diameter of Males Between 1
and 48 Months of Age
FRANCIS E. JOHNSTON, MARIAN WESTON, SHORTIE MCKINNEY,
JAMES COLEMAN, GILBERT0 PEREIRA, AND JEAN ROUNDS
Department of Anthropology, University of Pennsylvania, Philadelphia,
Pennsylvania 19104 (EE.J., M. W, Department of Nutrition, Drexel
University, Philadelphia Pennsylvania 19104 (S.M.), Neonatology
Department, Children’s Hospital of Philadelphia, Philadelphia,
Pennsylvania 19104 (J.C., G.P., J.R.)
KEY WORDS
Fat cells, Growth, Body composition, Infancy
ABSTRACT
The mean fat cell diameter was determined from measurements of abdominal adipose cells, obtained during inguinal hernia repair, of
126 white and 95 black males ranging in age from 1through 48 months of age.
The mean diameters of black and white subjects did not differ significantly,
suggesting that differences in fatness among adults of these two ethnic groups
have their origin beyond the age range of this study. The mean fat cell
diameter increased through the 6-8-month age group, decreased until the end
of the first year, and then levelled off through 48 months of age. Comparison
of this curve with those for the triceps, subscapular, abdominal, and suprailiac
skinfolds of the same subjects showed generally parallel courses except for the
triceps, which continued to increase in size after the means of fat cell diameters
and the other skinfolds had levelled off. Our data indicate that changes in body
fatness on the trunk at least in the first 4 years of life may be accounted for by
changes in fat cell size.
The development, in the 1970s, of techniques for the characterization and quantification of adipose tissue cellularity stimulated
a wide-ranging body of research into methodological issues, as well as applications of
the findings to clinical and epidemiological
areas of research. In particular, the discovery
of increased adipose cell size and number
among the obese (Bray, 1970; Hirsch and
Knittle, 1970; Brook and Lloyd, 1973; Sjostrom and Bjorntorp, 1974)resulted in a surge
of interest in the subject both in professional
and popular publications. During this period,
research and speculation led to the formulation of the “adipocyte number hypothesis,”
which postulates that the number of adipocytes is fixed early in life due to environmental andor hereditary influences (Roche,
1981). The result of this early fixation is to
“predestine” individuals towards a lifetime
of obesity or leanness. While the implications
of this hypothesis are clearly important and
while they have enjoyed immense popularity, it is clear now that the adipocyte number
hypothesis must be viewed with considerably
more caution than was originally the case.
0 1984 ALAN R. LISS. INC.
Sjostrom et al. (1972) have described differences among male and female adults of different ages, as well as among anatomical
sites within the same individual. By transplanting cells of mice from site to site, Meade
and Ashwell (1979) demonstrated that site
differences resulted from location on the body
rather than in the sample of fat tissue itself.
In his review of age changes during development, Brook (1978) has suggested that, at
present, methodological difficulties prevent
any reliable estimates of adipocyte number
in a n individual.
Summarizing the available data, Roche
(1981) concluded that, based upon present
knowledge, the adipocyte number hypothesis
is untenable. In large part, this is due t o
methodological problems involved in the estimation of body fatness a t the whole body
level, and to the extrapolation of measurements of adipocytes from a single region (or
even from several regions) to the entire adipose organ. Additional data are required before the important questions raised by
research conducted to date can be answered.
Received January 9,1984;accepted July 31, 1984
342
F.E. JOHNSTON ET AL
In this paper we present data on age differences in the mean size of abdominal adipose
cells from a sample of 221 black and white
male infants and young children. The information should contribute to our knowledge of the growth of adipocytes during this
potentially crucial period of human development.
MATERIALS AND METHODS
The data analyzed in this paper are taken
from a comprehensive mixed-longitudinal
study of the growth and development of infants and children from the Greater Philadelphia area. Subjects were drawn from those
males 48 months of age and younger who
underwent surgery for repair of an inguinal
hernia a t the Children’s Hospital of Philadelphia from August 1, 1979 through February
28, 1981. In view of the low incidence of hernia among females, we have restricted our
sample to males.
At the time of surgery, a sample of subcutaneous tissue was collected at the point of
incision. Following the method of Sjostrom et
al. (19711, the tissue was frozen after a brief
period of fixation in formaldehyde, sectioned,
and mounted for photomicrography. The photomicrographs were enlarged to a standard
size and a n average of 56 cells were traced
for each individual. The circumferences of
the cells were then measured with a planimeter, converted by computer to diameters,
and expressed for analysis in microns. Systematic scanning procedures were followed
to prevent bias in selecting cells for tracing.
Virtually all of the 12,000+ cells were traced
by one research assistant and all circumferences were measured by another. Inter- and
intraobserver reliability for both tracing and
measurement were analyzed and found to be
quite high. Usable adipocyte measurements
were obtained from 221 subjects, 126 white
and 95 black, ranging in age from 1through
48 months of age.
A battery of additional information and
measurements was collected a t the time of
surgery. This included anthropometry
(growth and body composition), sociodemographic data, and information on dietary intake and preferences. Those subjects under
12 months of age were enrolled in the longitudinal component of the study, to be visited
in their homes at 6 (if appropriate), 12, 18,
and 36 months of age. At these follow-up
visits anthropometric data were collected, as
well as similar measurements of siblings and
the subject’s mother. In addition we have
collected dietary recalls and histories, food
preferences of the mother, maternal ratings
of child temperament at 6,18, and 36 months
(Carey, 1970; Carey and McDevitt, 1978),
and, in a subsample at 18 months, records of
heart beats and sleeplwake patterns over a
%-hour period.
In view of the increased incidence of shorter
gestational ages associated with inguinal
hernia (Czeizel, 1980),all ages have been adjusted for gestational age as verified from the
hospital records at birth. For this paper, subjects have been grouped into eight groups, as
shown in Table 1. These particular age
groupings were chosen for two reasons. First,
we optimized our age distribution of subjects,
giving us sufficient numbers per cell. Second,
the groups correspond in general to the rate
of postnatal growth, providing larger numbers a t ages when growth velocities are
highest.
For this paper we are reporting only on the
analysis of fat cell diameters and anthropometry at the first, i.e., the surgery, visit. Subsequent publications will utilize the
longitudinal component as well as the other
data collected as part of this study.
RESULTS
We examined the shapes of the distributions of fat cell means in each of our subjects.
This was done visually as well as by the
calculation of the 3rd and 4th moments about
the mean. As might be expected, a range of
variability was found in skewness and kurtosis. However, the majority of distributions
did not depart significantly from the normal
in skewness and, as a result, we have chosen
to utilize the mean and standard deviation
for description and parametric statistics for
analysis.
Table 1presents the number of subjects, by
race, in each age group, and, for the fat cell
diameters, their means, standard deviations,
and coefficients of variation. An analysis of
black and white subjects, adjusted for age,
revealed no significant differences in the
means (F’ = 0.79, p = 0.37) and, as a result,
we have pooled the two racial groups to increase sample size and resulting power.
There is considerable variation within any
single age group, with coefficients of variation ranging from 11.4 to 22.2%. The smallest standard deviation, 7.86, occurs among
FAT CELL SIZE AND GROWTH
343
TABLE 1. Mean fat cell diameter in Philadelphia male infants and children
Age
group (mo)
Black
Sample size
White
B-2
11
3-5
6-8
9-11
12-17
18-23
24-35
36-48
34
12
9
10
7
5
20
22
8
8
18
13
18
19
Total
95
126
I
the youngest subjects, this value being significantly less than the next smallest SD,
11.95 a t 3-5 months (F = 2.31, p = .004).
The means show a n increase in fat cell
diameter from the youngest group, birth to 2
months, through the 9-11-month group. The
difference between the B-2 and 3-5 month
means is significant (t = 2.65, df = 85, p <
.01) as is that between the 6-8- and 9-11month means (t = 2.18, df = 43, p <.05).
Following the 9-11-month group, the means
decrease and level off, showing no significant
differences among themselves.
The changes with age may be verified by
calculating, within age groups, the correlation of mean fat cell diameter and age. To do
so, we obtain the following in the first 2 years
of life: B-5 months, +0.17; 6-11 months, 0.00;
12-17 months, -0.81, and 18-23 months,
-0.32.
Figure 1presents graphically the mean fat
cell diameter by age group. In addition we
have plotted the means for each of the four
skinfolds which were measured within 24
hours of surgery. The shapes of the curves
for the subscapular, abdominal, and suprailiac skinfolds generally parallel that for the
mean fat cell diameter, with increasing values in the first year of life, followed by a
decrease and a levelling-off by 18 months.
From 24 to 48 months, the means of these
four skinfolds show, overall, a slight decrease, something which is not seen in the
fat cell measurements.
The triceps skinfold means do not conform
to the above observations. While there is the
increase in the first year and a subsequent
decrease, there is a general increase in the
means from the 12-17-month group through
the age range of the study.
Total
Mean
31
56
20
17
28
20
25
24
68.5
74.8
73.8
77.0
68.0
70.2
70.1
69.6
22 1
Fat Cell Diameter (pm)
S.D.
cv (%)
7.86
11.95
16.39
13.09
13.90
14.03
11.86
13.80
11.4
16.0
22.2
17.0
20.5
20.0
16.9
19.8
10 u
mm.
2.
1.
mg.
One particular observation distinguishes
the fat cell means from each of the skinfold
thicknesses. The mean fat cell diameter is
greatest in the 9-11-month group. This value
is, as noted above, significantly greater than
the subsequent 12-17-month mean, but not
different from the preceding 6-8-month value
(t = 0.66, df = 35, p > .40). In contrast to
this, the largest mean for each of the skinfolds occurred in the 6-8-month group.
DISCUSSION
As noted earlier, in recent years, doubt has
been cast upon the validity of current measures of adipose cell number as indices of
hypercellularity in individuals. For example,
in a study of the adipose cells of 80 obese and
27 nonobese individuals, Jung et al. (1978)
found a slight increase in the estimated num-
344
F.E. JOHNSTON El' AI,.
ber of fat cells of the obese; however, no relationship existed between cell number and the
age at onset of obesity. Based upon differences in the mean size of subcutaneous and
omental cells, they concluded that the techniques for counting which are used a t present result in a n underestimate of cell
number. This suggests that the obese may be
able to accommodate increased amounts of
fat without adding new cells.
Kirtland and Gurr (19791, after reviewing
the published evidence, reached a similar
conclusion. While recognizing that the obese
do have more fat cells than the nonobese,
they suggest that this is a consequence, and
not a cause, of the obesity.
Based upon the literature, we have chosen
to focus our study upon cell size, a variable
which can be measured with much greater
reliability as well as validity. Even so, the
measurement of adipose cell size presents
methodological difficulties. Of particular
concern is the degree to which a sample of
adipose tissue from one site is representative
of other sites throughout the body. Issues
related to the protection of human subjects,
especially infants and children, precluded our
taking concurrent samples from other sites.
However, some data on variation among sites
are available in the literature. In a study of
24 adults in their 20s, Sjostrom et al. (1972)
found, among 11males, correlations between
weights of fat cells from different anatomical
regions ranging from 0.43 to 0.56. The exception to this range in their study was the
correlation of epigastric and hypogastric fat,
at 0.81. Except for the last, these coefficients
were not significant because of the very small
sample size. If we assume that the values
would remain the same, they would achieve
significance at the .05 level with a sample
size of 21. Even so, the correlations are only
moderate and leave considerable variance
unexplained.
The age-associated patterns of our data are
generally consistent with the findings of
Boulton et al. (1978)in a study of a sample of
43 infants and fetuses through 28 months of
age. Using the modal cell diameter for analysis, they found a n increase until 6-8 months
of age, with no further changes. The mean
diameters of our subjects increased in a similar fashion, but showed somewhat smaller
means from 12 through 48 months.
The age-related patterns of the fat cell
means agreed quite well with the patterns
for the skinfolds which were measured, the
least so with the triceps. This general agreement suggests that the increase in body fatness between early infancy and 48 months of
age, as indicated by skinfold thicknesses, can
be accounted for by an increase in adipose
cell size. However, two exceptions to this observation exist. The first is the increase in
the means of the triceps fold after the 12-17month group, which was not noted for fat cell
diameter. One possible explanation is that
this reflects differences in limb fat, estimated
by the triceps fold, and trunk fat, from which
the adipose sample was taken.
The second exception to the above observation is in the disagreement between the skinfolds and the fat cell means in the age at
their peak value. For all skinfolds, this occurred in the 6-8-month group while the 911-monthmean was the highest fat cell mean.
Sampling or measurement error are always
possibilities. Some studies have found the
peak values for skinfold thinkness during
infancy to occur somewhat earlier, while still
others have failed to note any peak at all
(Johnston, 1978). Because of the lack of comparative information, we cannot speculate on
the significance in our data, if any, of the
difference between the ages at which the
peaks values for mean fat cell diameters and
mean skinfold thicknesses occur.
Based upon a longitudinal study of adipocyte development, Hager et al. (1977) suggested that increased body fatness can be
explained by an increase in fat cell size from
1-12 months, but by fat cell number from
12-18 months. Our cross-sectional data, if
correct, suggest that the increase in trunk
fatness during the first 4 years of life may be
accounted for by a n increase in fat cell size,
with the possible exception of the last part of
the first year of life.
Our data indicate no difference between fat
cell diameter of black and white subjects.
Neither were there differences in skinfold
thicknesses. While our sample sizes are
small, this is in agreement with the study of
Johnston and Beller (19761, who found no
differences in the triceps and subscapular
skinfolds of black, white, or Puerto Rican
newborns. Since it is well-established that
the levels of fatness of black American children, youth, and adults are less than those of
their white age and sex peers (Johnston et
al., 1972, 19741, it seems clear that factors
responsible for these differences are not expressed until after early childhood. With respect t o fat cell size, the findings of our study
FAT CEI,I, SIZE A N D GROWI’H
regarding racial differences are consistent
with anthropometric data.
Finally, we must emphasize that our findings may be generalized to normal-weight
infants and children, and not to the obese.
None of our subjects could be classed unambiguously as obese. Consequently, any conclusions or suggestions growing out of this
analysis may not be applied to obese infants
or children, whose fat cells may develop
within a different set of environmental andi
or hereditary determinants.
ACKNOWLEDGMENTS
This research was supported in part by
USPHS Grant HD-12480. The assistance of
Adrienne Rogers, Judy Ricci, Marc Hurowitz, and Charles White is gratefully recognized. This paper was presented a s part of a
symposium, “Adiposity Through the Life
Cycle,” organized by L.S. Adair and F.E.
Johnston, at the annual meeting of the
American Association of Physical Anthropologists, Indianapolis, April 8, 1983.
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