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Formula-fed and breast-fed baboons Weight growth from birth to adulthood.

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American Journal of Primatology 16:131-142 (1988)
Formula-Fed and Breast-Fed Baboons: Weight Growth
From Birth to Adulthood
DAVID M. GLASSMAN' AND ANTHONY M. COELHO, JR.'
'Department of Sociology and Anthropology, Southwest Texas State University, Sun Marcos;
2Behauioral Medicine Laboratory, Southwest Foundation for Biomedical Research, Sun
Antonio, Texas
The objective of this study was to compare the immediate and long-term
effects of type of infant diet (formula-fed vs. breast-fed) on the weight
growth of baboons. Longitudinal (serial) weight data were collected from
44 savannah baboons (Papio cynocephalus anubis) for the total preadult
period of growth from birth to approximately 8 years of age. Fifty percent
of the sample (11 females and 11 males) were fed a standard infant
formula by a nursery care technician for the first 18 weeks of postnatal
life. The remaining 11 females and 11 males were breast-fed by their
mothers for an equivalent period of time. After 18 weeks of age the
animals were removed from their infant environments (either nursery or
mother-reared) and assigned to one of four age-cohort social groups. Each
age-cohort group was balanced for infant treatment and gender. The
animals remained in these social groups for the duration of the project and
were provided nutritionally identical postweaning diets. No significant
weight differences were found between the two rearing conditions for
either gender during the initial 15 weeks of growth. Following this period,
however, females of breast-fed environments averaged greater weight at
all ages than their bottle-fed peers. The intensity of the adolescent growth
spurt was also slightly greater among the female breast-fed group. No
postinfant average weight-per-age disparity was observed between the
male treatment groups.
Key words: breast-feeding, bottle-feeding, infant nutrition, baboons
INTRODUCTION
Studies that compare the growth of children who are breast-fed with growth of
children who are formula-fed have arrived a t mixed, and often contradictory,
conclusions. For example, Fomon [19741, DeSwiet et al. [1977], Holly and Cullen
119771, and Bindon 119841 report that bottle-fed children demonstrate infant
weight growth that is greater than comparable breast-fed infants, while Sveger
[1978], Dine et al. [1979], Yeung et al. [1981], Pomerance [1987], and others have
found no difference in the weight growth of formula-fed and breast-fed
Received October 9,1987;revision accepted June 1,1988.
Address reprint requests to D.M. Glassman, Ph.D., Department of Sociology and Anthropology,
Southwest Texas State University, San Marcos, TX 78666.
0 1988 Alan R. Liss, Inc.
132 / Glassman and Coelho
children. The disparity in results between these two groups of studies may be the
result of a lack of standardization of conditions by which human infant rearing
practices are defined as being either breast-fed or formula-fed [Himes, 1979;
Bindon, 19841. The information provided by these studies of human children is
further complicated by other variables such as variation in prenatal maternal care,
socioeconomic background of the household, variations in formula make-up, and
differences in early infant care and stimulation. These variables are generally
acknowledged as being difficult to control in studies of human infant growth;
however, it is also recognized that these variables may potentially confound
results. Experimental studies of humans are limited by many methodological
limitations and ethical considerations; however, appropriate use of animal models
provides an alternate means of experimentally investigating the questions raised
in human studies.
Many different species have been used in prospective studies to model the
effects of environmental and genetic variables on growth and development. For
example, research on rodents has produced most of the experimental data that are
available on the role of early caloric intake in the development of adult adiposity
in an animal model. However, there is no convincing evidence that the rat data are
applicable to either humans or other primate species [Tanner, 1963, 19781. For
example, the findings of the early rodent studies by Hirsch and his colleagues
[Hirsch et al., 1966; Knittle & Hirsch, 1968; Czajka-Narins & Hirsch, 1974; Hirsch
19751on the effects of nutrition on fat cell number are being challenged by Lewis
et al.’s [1983,1984,1986] recent studies, which use nonhuman primates. The latter
studies provide evidence indicating that preweaning caloric intake has little or no
influence on the number of fat cells that are present at the age of weaning in
baboons. Rather, the size of the fat cell reflects overfeeding and is characteristic of
overfed adolescents and adults.
It is generally accepted that nonhuman primates are the most appropriate
animals to model the processes involved in human growth because humans and
nonhuman primates are genetically, physiologically, and behaviorally more similar to each other than they are to any other animal species. Baboons (Papio sp.)
are particularly useful as models of human growth and development. Their
patterns of normal growth and development are well documented from birth to
adulthood [Coelho et al., 1984; Coelho, 1985; Coelho & Glassman 1984; Glassman
& Coelho 1986a,b, 1987; Glassman et al., 1984; Lewis et al., 1983, 1984, 1986;
Rutenberg et al., 19871. These studies (and additional longitudinal research
carried out by our research team since 1974) indicate that baboons and humans
exhibit similar growth patterns. For example, baboons are among several species
of nonhuman primates that exhibit an adolescent growth spurt absent from the
growth pattern of rodents [Watts & Gavan, 1982; Coelho et al., 1984; Glassman et
al., 1984; Coelho, 19851. The adolescent period is important because, like infancy,
it is a critical period of rapid growth that directly precedes the attainment of final
adult size. In baboons, adolescence begins at approximately 3.5 years of age, and
adulthood is attained at approximately 7 (females) to 8 (males) years of age; thus
baboons develop approximately three times faster than humans [Coelho, 19851.
Moreover, Lewis et al. 11983,1984, 19861 and Rutenberg and Coelho [19881 have
experimentally demonstrated that differences in caloric intake affect baboon
growth during infancy. Use of animal models in prospective experimental studies
of growth are important because they can provide information on the roles of
genetics and environment in the development of obesity or other growth disorders.
In this paper we build upon our previous studies of the baboon model of human
growth and development [Relethford et al., 1982; Lawrence et al., 1982; Glassman
Growth in Formula-Fed and Breast-FedBaboons / 133
& Coelho 1986a,b, 1987; Coelho & Glassman 1984; Glassman et al., 1984;
Rutenberg & Coelho, 1988; Rutenberg et al., 19871 by presenting results of an
experiment designed to assess the impact of breast feeding versus formula feeding
on the pattern of growth in weight from infancy t o the onset of adulthood in a
sample of baboons. The objectives of the study were to 1)describe and compare the
growth in weight attained for two infant treatments (breast vs. formula) during
infancy and in subsequent age periods leading to adulthood; 2) assess the effect of
treatment on the timing and intensity of the adolescent growth spurt; and 3) assess
the effect of treatment on the timing of menarche for females.
MATERIALS AND METHODS
Subjects
The 44 baboons (Papio cynocephalus) used in this study were born by natural
delivery at the Southwest Foundation for Biomedical Research in San Antonio,
Texas. The 44 subjects were studied from birth to approximately 8 years of age.
This period encompasses the normal subadult growth period for weight, crownrump length, and dental eruption for this species [Coelho, 1985; Glassman et al.,
19841. Each animal was born to a different mother. Diet, social environment, and
prenatal care of all mothers were identical. Six sires were responsible for the total
sample, with each sire contributing approximately equal numbers of progeny. The
offspring of each sire were assigned to both infant diet treatments to minimize
genetic effects in the overall association of infant diet and weight growth.
Infant Environments and Diets
Infants were assigned to one of two rearing environments within 24 hours of
the natural birth. A total of 22 animals (11females and 11males) were assigned
to the nursery environment under human care and were fed an equivalent human
infant formula prepared by Ross Laboratories. Nursery-reared infants were fed
five times a day for the first 2 weeks, four times a day for the next 2 weeks, and
three times a day until approximately 14 weeks of age when weaning from the
formula diet to the solid diet began. Peer-group socialization was provided for
nursery animals during a 2- to-3-hour period each day. The remaining animals (11
females and 11 males) were housed together with their mothers in large outdoor
caging, and the infants were breast-fed by their mothers. These mothers typically
began weaning their infants between 14 and 18 weeks of age, at which time infants
began sampling the diet consumed by their mothers (standard primate laboratory
diet). Subjects remained in their respective infant environments for 18 weeks.
Baboon milk [Buss, 19681 and the prepared infant formula were very similar.
Both had 16 g per liter of protein; the formula diet had 37 g per liter of fat and 70 g
per liter of carbohydrate compared to 50 g per liter of fat and 73 g per liter of
carbohydrate in baboon milk. The cholesterol content of the infant formula was
approximately 2 mg/dl.
Postweaning Environment and Diet
After 18 weeks of age, the animals were removed from their infant environments (either nursery or mother-reared), and four social groups were formed by the
introduction of an approximately equal number of males and females and approximately equal numbers of breast-fed and formula-fed individuals. The animals
remained in their assigned groups for the duration of the approximately 8-year
project. Each social group was housed in a large outdoor cage measuring
134 I Glassman and Coelho
12 x 5 x 5 m (L x W x H). This facility provided adequate room for
species-typical levels of activity.
All animals were provided ad libitum a diet whose caloric content was
approximately 22% from protein, 40% from fat, and 38%from unrefined carbohydrates. The diet consisted of Ralston-Purina Special Monkey Chow 25 5045-6 with
vitamin supplementation and added fat. The exact nature, composition, and
analyses of the diet (fat type and cholesterol components) are described in detail by
Mott et al. [1978, 19821 and McGill et al. [19801. These dietary specifications
approximate the range of an average American diet.
Data Collection
Longitudinal (serial) weight records were maintained on each animal beginning a t birth and continuing at 3-week intervals for the initial 15 weeks and at
12-week intervals beginning from the 28th week to the end of the study. Animals
were weighed on a self-balancing scale large enough to accommodate the entire
subject. Measurements were taken to the nearest gram a t ages 1year or younger
and to the nearest tenth of a kilogram at ages older than 1year. After attaining
approximately 6 months of age, animals were sedated with ketamine hydrochloride a t the standard dosage of 10 mgtkg prior to weighing. Females were tubally
ligated after menarche in order to remove the effects of pregnancy on weight
growth while allowing for normal sexual cycling. Age of menarche (defined as the
first observed menses) was recorded for all females and was known from daily
observation of all study subjects.
Data Analysis
Males and females were treated independently as were the two infant diet
treatments for all analyses. Mean values for weight were calculated at each
sampled age and compared by gender and treatment (breast vs. formula) group.
Distance growth curves were plotted from mean values of weight attainment
against age [Sinclair, 19691. The Student t-statistic was used t o test for significant
differences in weight between the two treatment groups a t approximately 8 years
of age for males and a t approximately 7 years for females, the age a t which initial
adult weight was estimated to be attained. Initial adult weight was defined as the
age immediately preceding the first negative average increment (or at the age of
lowest average increment) coinciding with the average age of completed dental
eruption in baboons (eruption of third molars-Coelho, unpublished data).
The rate of weight growth was described by mean weight gains for each 3-week
interval during the initial 15 weeks of postnatal growth, and by mean weight gains
for each 12-week interval beginning at 28 weeks. Mean weight gains were
calculated as
X
Y= XX,
+ 12 weeks - X,
,
(1)
X
where
and x
P
=
= mean weight gain for a given 12-week interval, X,
number of individuals.
=weight
a t age n,
No attempt was made to estimate missing values (i.e., only individuals represented
by both data points were included in the mean weight gain calculation for any
interval).
We tested the following null hypotheses:
Growth in Formula-Fedand Breast-FedBaboons / 135
0 . 3 4 . .
o
, . . . . .
.
a
e
12
,
13
-
*
18
. ,
OR
0
3
3
6
R0
AGE m WEEKS
12
e
s
12
1
13
1s
,
. ,
AGE W WEEKS
AGE M WEEKS
Od
l 0
.
. . . , . . . , .
1s
1G
8
O R A . ,
0
3
. ,
6
.
,
0
.
,
12
.
15
18
AGE W WEEKS
Fig. 1. Distance and increment weight gain curves for males and females during infancy (a = distance curves
males; b = increment curves males; c = distance curves females; and d = increment curves females).
H01: There are no significant treatment (breast vs. formula) effects on
weight growth at weaning (15 weeks of age).
H02: There are no significant treatment (breast vs. formula) effects on
weight attained at the onset of adulthood.
H03: There are no significant treatment (breast vs. formula) effects on the
timing of the onset of menarche in females.
Student's t-statistic was used to test the hypotheses. An alpha level of .05 was
chosen as the criterion for significant rejection of the null hypothesis for all
analyses.
RESULTS
Distance and Average Increment Curves: Infant Treatment Period
Distance and average increment curves for weight gain during the rearing
treatment period (i.e., the first 15 weeks of life) are presented for males and
females in Figure 1, while descriptive statistics are provided in Table I. Mean
weights of breast-fed males were greater than their formula-fed peers at each age
sampled (Fig. la). The magnitude of difference a t 15 weeks, however, was not
significant. The average increment curve for breast-fed males (Fig. lb) was
irregular in pattern and alternated from decreasing to increasing rates. Formulafed males had an average increment curve of uniformly increasing rate from birth
until 9 weeks followed by a decreasing rate of growth to week 15, yielding a near
parabolic-shaped curve. This declining growth rate may reflect the increasing
136 / Glassman and Coelho
TABLE I. Average Baboon Weights (kg) During Infancy
Age
(weeks)
Breast-fed
Formula-fed
N
x
SD
SEM
N
x
SD
SEM
11
10
11
11
10
11
0.92
1.19
1.32
1.63
1.78
1.8
0.08
0.13
0.18
0.18
0.17
0.20
0.02
0.04
0.05
0.06
0.05
0.06
11
10
11
11
11
11
0.92
1.00
1.19
1.41
1.61
1.73
0.17
0.22
0.25
0.28
0.26
0.25
0.05
0.07
0.08
0.09
0.08
0.08
10
9
11
11
10
11
0.86
1.03
1.16
1.28
1.41
1.59
0.12
0.15
0.15
0.18
0.19
0.31
0.04
0.05
0.04
0.06
0.06
0.09
11
11
11
11
10
11
0.85
0.92
1.08
1.28
1.48
1.59
0.18
0.17
0.19
0.18
0.17
0.24
0.05
0.05
0.06
0.05
0.05
0.07
Males
0
3
6
9
12
15
Females
0
3
6
9
12
15
inadequacy of formula as the animals get larger or some natural variation in
growth rate.
Females demonstrated minimal infant diet effect in their growth pattern from
birth to 15 weeks (Fig. lc,d). The distance curves of breast-fed and bottle-fed
females were virtually identical with both groups averaging 1.59 kg at 15 weeks of
age. The average increment curve for breast-fed females was characterized by a
constant average rate of 0.13 kgl3 weeks from birth to 12 weeks, followed by an
average increase of greater than .2 kg for the next 3-week interval. The average
increment curve for formula-fed females closely paralleled the near parabolicshaped growth pattern of formula-fed males.
Distance and Average Increment Curves: Postweaning Period
Postweaning growth for male baboons followed a sigmoid pattern (Fig. 2). The
pattern was shared by males of both infant treatments. The magnitude of weight
differences a t any sampled age was not considerable. No significant difference was
observed in initial adult weight at 400 weeks (7.7 years) of age.
The pattern of average increment curves between the two groups of males was
also similar (Fig. 3a), yet the timing of peak growth rate during the adolescent
growth period differed. Both groups of males began their adolescent period of rapid
growth a t approximately 196 weeks (3.8 years) and continued this pattern for
approximately 104 weeks. Peak growth rate for breast-fed males occurred at week
268 (5.2 years) with an average of 2.1 kg/12 weeks. Formula-fed males achieved
peak growth 12 weeks later at week 280 (5.4 years) where they averaged a gain of
1.9 kg112 weeks. Following the period of rapid growth, both treatment groups
exhibited an irregular pattern of growth rate deceleration.
The distance curves for female weight growth were more linear than the
distance curves for males (Fig. 2). Breast-fed females averaged greater weight than
their formula-fed peers a t all postweaning ages sampled. Unlike the males,
females showed a generalized pattern of continual increase in weight disparity
between the two treatment groups with advancing age until week 340 (6.5 years),
at which time the formula-fed females caught up to the attained growth of the
breast-fed females [see Rutenberg & Coelho, 19881. No significant weight
Growth in Formula-Fed and Breast-Fed Baboons / 137
20
-
10
-
MALE-BREAST
MALE-BOTTLE
+ FEMALE-BREAST
+ FEMALE-BOTTLE
Q
+
0
!
0
.
1
5 2
. l . 1 . , . , . , . , . 1
104 156 208 260 312 364 416
AGE IN WEEKS
Fig. 2. Postinfancy distance curves of weight growth for males and females.
disparity was observed at the time of initial adult weight between the two
treatment groups.
The average increment curves for females indicated a general pattern of
increased growth rate for breast-fed females over their formula-fed peers during
the initial two-thirds of the postnatal growth period (Fig. 3b). The increment
curves suggested that the onset of rapid growth occurred at a similar age for the
two treatment groups. The timing and magnitude of peak growth rate, however,
differed with breast-fed females achieving peak rate at week 196 (3.8 years) with
an average increase of 1.3 kg/12 weeks, compared to formula-fed females, which
achieved peak rate at week 220 (4.2 years) and an average of 1.0 kg/12 weeks. The
period of rapid growth persisted in both treatment groups for approximately 1.4
years. Following this period, weight growth for breast-fed females decelerated
uniformly, whereas formula-fed females exhibited an irregular pattern of growth
with growth rate exceeding the breast-fed group a t most ages sampled. Within this
terminal period of postnatal growth, formula-fed females converged on the weightper-age attainment of breast-fed females.
Comparison of Age at Menarche
The average age of menarche was 183 weeks (3.5 years) for breast-fed females
compared to 189 weeks (3.6 years) for their formula-fed peers. The average
difference between the two treatments of 6 weeks was not statistically significant
(Table 11). The overall variability in the onset of menarche ranged from 141 weeks
(2.7 years) for early-maturing females to 214 weeks (4.1 years) for late-maturing
females.
DISCUSSION
The results of this study indicated that baboon weight growth during infancy
was not affected by feeding either breast-milk or formula, despite the fact that
breast milk was provided by mothers and formula was provided by nursery
technicians. Moreover, the pattern of postweaned weight growth was similar
138 / Glassman and Coelho
3a
MALE-BREAST
Q
- 1 ! .
I
0
52
.
,
*
104
.
,
156
,
. , .
208
260
I
312
.
I
.
364
I
416
AGE IN WEEKS
3-
3b
Q
FEMALE-BREAST
-+ FEMALE-BOTTLE
2-
1-
0-
- 1 ! .
0
, . ,
52
104
.
I
156
.
I
208
.
I
260
.
1
312
. , .
I
364
416
AGE IN WEEKS
Fig. 3. Postinfancy increment weight gain curves for males (a)and females (b).
among the two groups. What appears to differ primarily was the rate of maturation
for females. Postweaned breast-fed females exhibited, on average, a greater
weight-for-age than their formula-fed peers until the latter group catches up
during the final phase of subadult growth.
The apparent disparity in female weight growth, occurring after infancy when
the animals were fed nutritionally standardized diets, may be related to one or
Growth in Formula-Fedand Breast-Fed Baboons / 139
TABLE 11. Age of Menarche in Breast-Fed and Formula-Fed Female Baboons
Ape in weeks
~~
~
Infant diet
N
x
SD
Range
t
Breast-fed
Formula-fed
11
11
183
189
11.7
20.5
168-202
141-214
0.90
more factors exclusive of the possible statistical artifact of sample size and
repeated-measures effect. One explanation is the possibility of a deferred or
delayed nutritional effect. If correct, this effect is observed in greater weight-forage, increased rate of peak growth, and an earlier, although not statistically
significant, age a t menarche for the breast-fed monkeys. The dietary agent or
agents transmitted via the infant diet and responsible for the delayed or enhanced
effect on maturation remain unknown. The available infant formulas are not
identical with human breast milk in all aspects of their composition. Therefore, an
unidentifiable agent or combination of agents that differentiate breast-milk from
formula may be impacting on growth. It may also be proposed that human formula
may not be nutritionally optimal for baboon growth and therefore responsible for
the study’s outcome. However, we would suggest that this is unlikely because there
were no differences in the growth outcome of males in the study. Furthermore,
baboon milk is similar to human milk in containing less protein, fat, and minerals,
but more lactose than nearly all nonprimate mammals [Jenness & Sloan, 19701.
Human infant formula is nutritionally formulated to reflect this composition and
should be compatible with the biology of most anthropoids. For example, human
infant formula is considered a standard acceptable diet for rearing infant nonhuman primates in research centers and zoological parks.
A second possible cause of the treatment differences may rest in the role of
caloric expenditure resulting from behavioral activity. The role of behavioral
activity in the regulation of energy balance in primates, both human and
nonhuman, may be among the most important, most overlooked, and least
understood factors capable of altering growth in weight [Coelho, 19861. Although
there are many publications suggesting the importance of activity in caloric
balance, there are few empirical and prospective studies in the literature [Coelho,
19861. This lack of information is in large part due to the difficulties that these
types of studies pose for researchers. Behavioral activity is important because it is
a major component in energy regulation (i.e., performance of behavior requires
expenditure of energy). If there were significant and prolonged differences between
breast-fed and formula-fed females in the performance of behavior during the
period of growth described in this study, then it is possible that these differences
could account for observed differences in weight and in the timing of maturation.
This assumes that both groups consumed similar amounts of food and differed in
behavioral activity and subsequent energy expenditure. For example, it is possible
that formula-fed females were more active than breast-fed females (i.e., formulafed females may have been hyperactive relative to the breast-fed females). Thus,
while the formula-fed females expended energy in behavioral activity, breast-fed
females would have more calories available for growth of tissue.
It is also possible that the formula-fed animals learned to be more active as a
result of their first 15 weeks of experience in the nursery environment. If learning
were involved, then it raises the additional question of why females were affected
but not the males. It is highly unlikely that female subjects learned something in
140 / Glassman and Coelho
the nursery environment that the male subjects did not, as both groups were
reared according to the identical standardized protocol.
Our results suggest that an analysis of the possible effects of differences in
behavioral activity on growth from birth t o adulthood in primates may be an
important research topic that would require a major research effort and that could
provide extremely valuable information t o improve our understanding of processes
involved in growth.
CONCLUSIONS
1. No significant weight differences were observed between breast-fed and
formula-fed baboons of either gender at 15 weeks of age or a t adulthood.
2. Breast-fed animals tended to be heavier than their formula-fed counterparts during growth, but this tendency was more marked in males during the first
15 weeks and in females during the subsequent part of the growth period.
3. Breast-fed animals of both genders tended to have earlier and greater
maximal adolescent weight increments than their formula-fed peers.
4. Breast-fed females attained menarche on average earlier than did formulafed females although the difference between the mean ages of menarche was not
statistically significant.
ACKNOWLEDGMENTS
We acknowledge the assistance of Dr. K. Dee Carey and his staff for their help
in caring for the study subjects and maintaining the experimental protocol while
the baboons were in the nursery and in subsequent years while they were in the
colony; Dr. Gary W. Rutenberg for his helpful comments on the text; and the
members of the Behavioral Medicine Laboratory who participated in the collection
and processing of the morphometric data. This research and preparation of this
manuscript was supported by an Andrew G. Cowles Research Fellowship and by
grants from the National Institutes of Health NHLBI-19363 and NHLBI-28972.
Southwest Foundation for Biomedical Research is accredited by the American
Association for Accreditation of Laboratory Animal Care and is in compliance with
the requirements of the Animal Welfare Act.
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