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School of Dietetics and Human Nutrition and * Department of Physical Education, McGill University, Montréal, Québec, Canada H9X 3V9
3To whom correspondence and reprint requests should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • rats • lactose • exercise • lactation • milk fat
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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,
Koski and Hill 1986 and 1990
) and is also considered the
principal precursor for milk lactose and de novo synthesis of milk fat
(Koski et al. 1990
, Williamson 1980
). It
is thus conceivable that when daily energy requirements are increased
by regular exercise in untrained animals, a competition for glucose
could exist between the exercising muscle and either the developing
fetus or the lactating mammary gland. It is well established that
exercise training increases the muscle's capacity to mobilize and
oxidize fat and that there exists an increased burden on the energy
supply from glucose in untrained animals (McArdle et al. 1986
).
Previous studies have shown that acute exercise in untrained pregnant
rats diminishes maternal (Carlson et al. 1986
,
Gorski 1983
) and fetal liver glycogen reserves
(Gorski 1983
), compromises glucose uptake by the fetus
and is associated simultaneously with an augmentation in maternal
muscle glycogen concentrations (Treadway and Young 1989
). More recently, it has been observed that acute bouts of
exercise in the untrained pregnant rat dam, combined with restricted
maternal dietary glucose, compromised glucose delivery to the
developing fetus as evidenced by reduced concentrations of liver and
heart glycogen; however, the additional dietary restriction also
reduced maternal muscle glycogen concentrations (Cobrin and Koski 1995
). In trained rats, acute and chronic exercise
augmented maternal skeletal muscle glycogen content and the expected
decrease in maternal liver glycogen was prevented (Mottola and Christopher 1991
). Additionally, the increased fetal weights
showed that, despite increased glucose uptake in muscles of trained rat
dams, glucose delivery to the fetus was not compromised if the animals
were trained (Mottola et al. 1993
).
Lactation performance during exercise has not been as thoroughly
investigated. Only one study has tested the possibility that maternal
exercise alters glucose supply to the mammary gland during lactation
(Treadway and Lederman 1986
). Milk lactose was decreased
in trained rats fed a commercial nonpurified stock diet when swimming
exercise, begun 7 wk before pregnancy, was continued into lactation
(Treadway and Lederman 1986
). Decreased availability of
glucose to the mammary gland due to the increased energy requirement of
exercise and failure of the lactating rat dam to compensate for
increased glucose demand were among the suggested explanations for the
decrease in milk lactose. More recently, reports that maternal dietary
glucose was an important determinant of lactose (Koski et al. 1990
) and milk fat concentration (Lanoue and Koski 1994
) strongly support the possibility that maternal dietary
glucose is also important for optimal lactation performance. The
purpose of this study was to examine the following: 1)
whether regular bouts of low intensity exercise in untrained pregnant
rats limit glucose delivery to the fetus and thus compromise early
postnatal survival if maternal dietary glucose is limited; and
2) considering that glucose is required for milk lactose and
de novo synthesis of milk fat, whether the increased energy demands of
exercise could compromise lactation performance.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. Experimental design.
A 3 x 2 factorial design was used to investigate the effects of three levels of maternal dietary glucose (20, 40 and 60%) and two levels of activity (chronically exercised = E,4 rested = R) throughout gestation on pregnancy outcomes. Pregnancy measures included maternal weight, litter size and weight, and early neonatal survival. A 3 x 2 x 2 factorial design was used to investigate the effects of diet, exercise and litter size (n = 8 and 12) on lactation performance. Lactation measures included maternal liver and muscle glycogen concentrations, plasma glucose and insulin concentrations, mammary gland weight and composition, milk composition and pup growth.
Animals.
Female Sprague-Dawley rats (175–200 g, n = 113, Charles River Canada, St. Constant, Canada) were
individually housed in wire screen cages in a
temperature-controlled room (21 ± 2°C) with fluorescent
lighting (0700–1900 h). Rats were randomly mated with one of 13 males
and then randomly assigned to one of three diet groups (Table 1). Rats had free access to water and the diets throughout pregnancy
and lactation. On gestation day 19 (Gd 19), all pregnant rats
(n = 105) were transferred to maternity cages. At
delivery, the litter was weighed as a unit. During monitoring of
neonatal mortality from lactation day 0 to 2 (Ld 0–2), which is the
most critical period (Koski and Hill 1986 and 1990
),
handling of pups was minimized by culling litters to either 8 or 12
pups and weighing individual pups on Ld 3.
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During the first 18 d after their arrival and before the start of
the exercise regimen, all rats were acclimated, using a modified
protocol (Mottola et al. 1983
), to run on a multilane
motor-driven treadmill initially at 10 m/min, 5 min/d at 0% grade
and gradually increasing to 20 m/min, 45 min/d by d 18. Rats were then
divided into two activity groups (E or R, n = 54/group). Rats assigned to the exercise group continued to follow the
acclimation protocol daily until they were successfully mated, usually
within 1 wk, as confirmed by vaginal plugs. The presence of vaginal
plugs became the first counting day of gestation or gestational day 0
(Gd 0).
Pregnant E rats began their low intensity exercise protocol on Gd 1 and
ran 20 m/min, 60 min/d at 0% grade, 7 d/wk [~300 (kg ·
m)/d)]5
until Gd 20. Previously, exercise protocols of running at 20 m/min on a
10o incline for 1 h/d, 7 d/wk (Mottola et al. 1983
) and at 15.5 m/min on a 0° incline for 20 min/d, 7 d/wk
(Cobrin and Koski 1995
) were both described as mild
exercise protocols. Our exercise protocol, which fell between these two
intensities, was also described as mild and was without any training
effect (increased concentrations of soleus muscle succinate
dehydrogenase). Training has been observed only with progressive
conditioning protocols when pregnant rats ran at a final intensity of
30 m/min on a 10° incline for 1 h/d, 5 d/wk for 3 wk (Mottola and
Christopher 199l).
Dams did not exercise from Gd 21 to Ld 3 (the period of parturition) to allow monitoring of neonatal survival until litters were culled to 8 or 12 pups on Ld 3. Exercised dams resumed running at an intensity of 20 m/min, 45 min/d [~265 (kg · m/d)] beginning on Ld 3, increased to 20 m/min, 60 min/d, 7 d/wk [~360 (kg·m/d)] on Ld 5 and continued at this intensity up to and including Ld 14.
Diet selection and composition.
Experimental and control diets are summarized in Table 1
. Diets were
isoenergetic and provided 17.35 kJ of metabolizable energy/g dry
diet and 15% protein by weight as casein, which met the NRC
(1978
and 1995)
requirements. All vitamins and minerals were
provided in quantities that met NRC (1978)
requirements
for pregnant or lactating rats, whichever were higher.
The 60% glucose diet was chosen as the control diet because 60–62%
carbohydrate diets have historically been used as control diets for
pregnancy and lactation studies in rats (Cobrin and Koski 1995
, Fergusson and Koski 1990
, Koski and Hill 1986 and 1990
, Koski et al. 1990
,
Lanoue and Koski 1994
). A 20% glucose diet was chosen
as the minimum amount of glucose required to produce a litter of live
pups that would survive to Ld 15 (Lanoue and Koski 1994
), yet potentially result in metabolically compromised
dams. Previous observations had shown that rat dams fed comparable
glucose-restricted diets (12 and 24%) had lower liver and muscle
glycogen reserves (Cobrin and Koski 1995
) and lower milk
fat concentrations (Lanoue and Koski 1994
). The 40%
glucose diet was chosen because it would provide an intermediate level
of dietary glucose and fat.
Sample collection and analytical procedures.
Milk composition.
Milk samples were collected on Ld 15 in a postabsorptive state (fed) as
described previously (Lanoue and Koski 1994
).
Total milk protein concentration was determined as described by
Hartree (1972)
with the exception that 50
µL raw milk was first incubated at 37°C in 450
µL of 0.1 mol/L NaOH. Lactose concentration was
determined by the orcinol-sulfate reaction described by
Svennerholm (1956)
. Total lipids were determined by a
colorimetric sulfuric acid/vanillin reaction kit (Cat. No. 124 303,
Boehringer Mannheim Canada, Laval, Canada). To assess whether the main
experimental effects of diet, exercise or litter size produced
differing amounts of milk that could contribute to changes in the
concentration of milk lactose, lipids or protein, 24-h milk yields were
determined on Ld 12 using a modified version of the pup
test-weighing procedure (Treadway and Lederman 1986
)
by incorporating <4 h of pup and dam separation and imposing 1 h
restricted nursing. Milk production reportedly does not decline with
<4 h of separation (Hanwell and Linzell 1972
,
Reddy and Donker 1965
), but the pup weighing method may
produce a 25% underestimation of true or actual milk yield
(Dobenecker et al, 1998
) compared with tritiated water
techniques. Therefore our data were analyzed comparing "relative"
milk yields among our experimental main effect groups (diet, exercise,
litter size) and not absolute or true milk yield.
Mammary gland and other maternal tissue samples.
Immediately after collection of milk samples, rats were
reanesthetized and blood was withdrawn by cardiac puncture,
centrifuged (1500 g for 10 min) and the plasma
stored at -80°C. Liver, heart, soleus and plantaris muscles from the
hind leg, as well as mammary gland tissue were excised, weighed,
freeze-clamped in liquid nitrogen and stored at -80°C until
analysis. Total protein and DNA concentrations were determined by
modified methods of Hartree (1972)
and Burton (1956)
, respectively. Bovine serum albumin and calf thymus DNA
were used as standards. All tissue (mammary gland, liver, muscle)
glycogen concentrations were determined by a modified method of
Lo et al. (1970)
. Total lipid content of
freeze-dried mammary glands was determined gravimetrically after
grinding and extraction with chloroform/methanol using the method from
the Soxtec System HT2 (Tecator, Höganäs, Sweden). Plasma
glucose concentration was quantified by hexokinase determination (Cat.
No. 16–20, Sigma Diagnostics, St. Louis, MO) using an Abbot VP Super
System (Irving, TX). Plasma insulin was measured using an
125I insulin RIA coated tube kit (Cat. No. Ktsp-11002,
Immunocorp, Montréal, Canada).
Statistical analyses.
All data were tested for homogeneity of variances using Bartlett's
test (Steel and Torrie 1980
). Data sets with
nonhomogeneous variances were log transformed or, when this
transformation did not result in homogeneous variances, observations
were weighted by the reciprocal of the group variance. Variances of
"day" groups for daily pregnancy and lactation food intake
patterns of dams, as well as cumulative weight gain pattern were found
to be nonhomogeneous and were not made homogenous by log
transformation. Given that only effects within the same day and not
from day to day were to be compared, nonweighted data for each day were
analyzed. All values, except neonatal mortality, are reported as
least-square means (LSM) ± SELSM because the data were
not balanced. Log transformed data were reported as
back-transformed LSM without SELSM. All statistics were
performed using the SAS System for Windows v.6.10 (SAS Institute, Cary,
NC). The interaction between diet and exercise was tested for all data.
When a significant interaction was found, any significant main effects
of diet or exercise were not reported as significant for that outcome.
Significant differences were identified within diet or interaction
effects with Bonferroni's test for multiple comparisons. Minimum
acceptable probability of significance was P < 0.05.
Food intake and maternal weight patterns were analyzed using repeated measures ANOVA for mixed models. All pregnancy data were analyzed using a 3 x 2 ANOVA; (3 diets, i.e., 20, 40 and 60% glucose, 2 activity levels, i.e., E and R, and the interactions between diet and activity, diet and day, and activity and day were tested). Neonatal mortality was analyzed using GLIM (The GLIM System, Release 3, Oxford, England), a statistical package that analyzes nonnormally distributed categorical data.
All lactation data were analyzed using a 3 x 2 x 2 ANOVA (3 diets, 2 activity levels, 2 litter sizes, i.e., 8 and 12 pups, and the interactions between diet and activity, diet and day, activity and day, and litter size and day were tested). Pup weight pattern was analyzed using separate nested ANOVA for mixed models for each day of measurement.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Maternal food intake.
Neither maternal dietary glucose level nor chronic exercise
significantly affected cumulative maternal food intake at term or on Ld
15 (Table 2). However, there were significant diet x day and exercise
x day interactions (data not shown). From Gd 5 to 13 and Gd 18 to
20, dams fed the 20% glucose diet consumed less food per day than dams
fed the 40% and/or the 60% glucose diets. On Gd 20–21, E dams
consumed significantly more food per day than R dams. During lactation,
there was no exercise x day interaction, but there was a
significant diet x day interaction; on Ld 1, 6, 9 and 14, dams
fed the 20% glucose diet consumed significantly more than dams fed the
60% glucose diet. There was also a significant litter size x day
interaction such that from d 1 to 14, dams that nursed 12 pups consumed
significantly more food per day than dams that nursed 8 pups. This
litter size x day interaction resulted in a significantly lower
cumulative food intake for dams that nursed 8 pups compared with dams
that nursed 12 pups.
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Rats did not differ in prepregnancy body weight by diet or activity
level. At term (Gd 21), maternal dietary glucose did not significantly
modify maternal body weight; however, exercise resulted in
significantly lower maternal body weights (Table 2)
. There was a
significant effect of diet x day interaction on cumulative
maternal weight gain during pregnancy; from Gd 10 to 20, weight gains
of dams fed the 20% glucose diet were lower than those of dams fed the
40 or 60% diets (Fig. 1A
). There was also a significant exercise x day interaction
such that from Gd 16 to 20, R dams gained more weight than E dams (Fig. 1
B.).
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. Pregnancy performance, neonatal growth and mortality.
Maternal dietary glucose and chronic low intensity exercise did not
significantly modify litter size or cumulative neonatal mortality
through Ld 2 (Table 3). Total litter weight corrected for number of pups born differed
by diet such that dams fed the 60% glucose diet had litters that were
significantly heavier than dams fed the 20% glucose diet. Litter
weight of dams fed the 40% glucose diet was not different from that of
either the 20 or 60% diet groups. Mean birthweight of individual pups
was not affected by maternal dietary glucose or chronic low intensity
exercise (Table 3)
; however, on Ld 15, pups of dams fed the 40%
glucose diet were significantly heavier than pups of dams fed the 60%
glucose diet (Fig. 2A
). In addition, pups in litters of 8 were significantly heavier
than pups in litters of 12 on Ld 11, 14 and 15 (Fig. 2
B).
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Activity level and litter size did not independently modify milk
composition except for milk fat concentration, which was significantly
increased in the E dams compared with the R dams (Table 4). Milk fat concentration also increased significantly as maternal
dietary glucose increased from 20 to 40 to 60%. There were also
important interactions between maternal dietary glucose and chronic low
intensity exercise on milk lactose and protein concentrations. E dams
fed the 20% glucose diet had a significantly lower milk lactose
concentration compared with R dams fed the same diet, whereas no such
difference was found in the 40 and 60% glucose diet groups
(Fig.
3A). Additionally, E dams fed the 40% glucose diet had a
significantly higher milk protein concentration than R dams fed the
same diet, and this concentration of milk protein was similar to that
of E and R dams fed the 20% glucose diet. In contrast, R dams fed the
40% glucose diet had significantly lower milk protein concentrations,
which were similar to those of both E and R dams fed the 60% glucose
diet (Fig. 3
B). None of the differences in milk composition
could be attributed to differing quantities of milk because
"relative" milk yields were similar across diet and activity
groups (data not shown); however, as predicted by the pup
test-weighing method, these were only 75% of true milk yields.
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|
.
Despite the fact that chronic low intensity exercise increased milk fat
concentration, it did not affect milk energy per liter. Mammary gland composition.
Mammary gland composition was unaffected by maternal dietary glucose;
however, E dams had significantly lower percentages of mammary gland
fat than R dams (Table 5). Dams that nursed litters of 8 had lower mammary gland wet
weights, mammary gland weights as a percentage of body weight and
mammary gland protein concentrations than dams that nursed litters of
12.
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Neither maternal dietary glucose level nor chronic exercise affected
maternal plasma glucose concentrations on Ld 15, but dams that nursed
litters of 12 had lower plasma glucose concentrations than those that
nursed litters of 8. Plasma insulin concentrations were lower in dams
fed the 60% compared with the 20% glucose diet and in E dams compared
with R dams (Table 5)
.
A 20% glucose diet and chronic low intensity exercise independently
resulted in lower maternal liver glycogen concentrations on Ld 15
compared with feeding a 60% glucose diet and no exercise (resting),
respectively; however, liver glycogen concentrations of dams fed the
40% glucose diet were not different from the 20 and 60% glucose diet
groups (Table 5)
. Litter size did not affect liver glycogen
concentrations. Moreover, maternal muscle glycogen concentrations were
not affected by dietary glucose level, low intensity exercise or litter
size (Table 5)
.
Nursing 8 pups resulted in lower maternal liver weights, but higher plantaris weights (data not shown) on Ld 15 compared with nursing 12 pups. Maternal liver, soleus, plantaris and heart weights (data not shown) were not significantly affected by dietary glucose level or exercise, and soleus and heart weights were not affected by nursing different litter sizes.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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,
Lovelady et al. 1990
), cows (Lamb et al. 1979 and 1981
) and rodents (Karasawa et al. 1981
,
Treadway and Lederman 1986
) have investigated the role
of exercise during lactation, but conclusions have differed. In humans,
no adverse effects on milk composition or milk yield were noted when
trained women (predominantly swimmers) exercised vigorously
(Lovelady et al. 1990
), but in untrained women who
exercised only during lactation using rapid walking, jogging and
bicycling, significant increases in milk protein were seen and there
was the suggestion of reduced milk volume (Dewey et al. 1994
). Swimming, which is not a weight-bearing exercise,
and walking or jogging, which are, promote weight and body fat loss
differently (Caldwell, 1988
, Gwinup 1987
). Swimming differs from running in circulatory and core
temperature responses and in muscle groups used (Flaim et al. 1979
); these factors, in addition to training effects, could
have contributed to these findings. In animal studies, cows subjected
to pre- and postpartum treadmill walking, a weight-bearing
exercise, at different levels of intensity and duration showed that
milk yield was reduced at high exercise intensities (Lamb et al. 1979 and 1981
). Additionally, increased protein concentrations
were observed, which they concluded compensated in part for reduced
milk volume. In rodents, who like cows have high milk production rates,
researchers have observed no effect on milk yield, mammary gland or
offspring weight when mice ran <0.152 km/d, an extremely mild exercise
routine (Karasawa et al 1981
), but in trained swimming
rats (>2 h/d), lactose concentration was significantly lower than in
sedentary controls (Treadway and Lederman 1986
). Taken
together, the results from this limited number of studies do suggest
that chronic exercise could produce differences in milk composition and
milk yield. Our results, which used chronic, low intensity exercise in
untrained pregnant rat dams, further substantiated the previous
observations of increased milk protein and decreased milk lactose
concentrations during exercise. However, the differences in lactation
performance resulting when exercise was combined with significant
changes in diet additionally emphasize the importance of dietary
adequacy and composition, particularly lipid and glucose, to the
lactation-exercise relationship.
Our results showed the following important contributions of diet
composition to the lactation-exercise paradigm. The existence of
important interactions between maternal dietary glucose restriction and
chronic exercise, which modified milk composition but not milk yield,
suggested an exercise-induced adaptation in the mammary gland that
depended on the proportion of glucose-fat in the maternal diet.
First, a 20% glucose diet was insufficient for rat dams exercising at
low intensity; lactation was compromised because these exercised rat
dams produced milk with significantly lower lactose concentrations but
higher protein concentrations than rested dams fed the same diet.
Second, lower levels of dietary glucose also decreased milk fat
concentrations proportionately. Finally, the effect of graded levels of
maternal dietary glucose on pup growth in the first 15 d of life
showed that the heaviest pups were nursed by dams fed a moderate level
of carbohydrate (40% glucose), suggesting that the requirement
indicated by the NRC (1978
and 1995)
for a high level of
dietary carbohydrate (>60%) may not be optimal for the lactating rat
and that a higher fat, lower carbohydrate diet may be preferred. Each
of these findings is discussed in more detail.
Chronic exercise in our untrained rats also produced changes in
lactation performance that were independent of diet. Some were
expected, such as the decrease in mammary gland weight, which had been
reported previously (Mottola et al. 1986
), but the
increase in milk fat had not been described in any of the previous
lactation studies (Dewey et al. 1994
, Karasawa et al. 1981
, Lamb et al. 1979 and 1981
,
Lovelady et al. 1990
, Treadway and Lederman 1986
). Possible explanations for this discrepancy in milk fat
concentrations between our study and those of others may arise because
the type and intensity of exercise in the other studies did not promote
greater reductions in the amount of mammary gland fat in the exercised
groups in part because there were increases in energy intake during
exercise to compensate for the additional energy expenditure. Because
our chronic low intensity exercise lowered mammary gland fat and
simultaneously raised milk fat concentrations, we suggest that the
chronic weight-bearing exercise in untrained pregnant rats led to
decreased mammary gland fat on d 15 of lactation, which may have
contributed to changes in milk fat.
Milk fat is derived from two sources, the circulation and de novo
synthesis from glucose within the mammary gland (Williamson et al. 1984
). We observed independent increases in milk fat as
glucose increased in the maternal diet, supporting the established
dietary relationship between glucose and milk fat (Lanoue and Koski 1994
). These results showed that maternal dietary glucose
is critical to milk fat synthesis even with relatively high dietary fat
intakes. This previous study (Lanoue and Koski 1994
)
reported that, compared with a high carbohydrate diet (60% glucose,
~16% fat), dietary glucose restriction to 12 or 24% glucose with 35
and 30% fat, respectively, decreased milk fat to a level comparable to
the 20% glucose diet in this study; below 20–24% dietary glucose,
however, milk fat was not further decreased. Based on our novel finding
of a milk fat–exercise relationship, we propose that there may be
another important relationship among exercise, mammary gland fat
mobilization and milk fat concentrations by suggesting that the
increase in milk fat after exercise, which was statistically
independent of the dietary effect of glucose on milk fat, may be due to
increased mammary gland lipolysis that reportedly occurs during
lactation (Hamosh et al. 1970
). This increased
availability of plasma nonesterified fatty acids and triglycerides,
combined with chronic low intensity exercise in untrained pregnant rat
dams, may lead to increased mammary gland fat mobilization and enhanced
substrate availability for milk fat synthesis during exercise.
Increased glucose availability to the mammary gland during exercise
could also play a role in increasing milk fat in untrained rats because
of an apparent shunting of glucose from the liver to the mammary gland;
however, this requires investigation.
Our results showed an important statistical interaction between diet
and exercise on milk lactose concentrations with the addition of low
intensity exercise significantly decreasing milk lactose in rats fed
only the low carbohydrate (20% glucose) diet. Previously decreased
milk lactose concentrations were reported with severe dietary
carbohydrate restriction (Koski et al. 1990
,
Koski and Hill 1990
, Romsos et al. 1981
)
or swimming exercise (Treadway and Lederman 1986
).
Treadway and Lederman (1986)
first proposed that
increased energy requirements during exercise were a possible cause for
the decreased milk lactose because the required glucose was diverted to
fuel maternal muscle. In this study, only the statistical interaction
between exercise and a carbohydrate-restricted (20% glucose) diet
and not the main effects of dietary glucose level or exercise decreased
milk lactose, suggesting that dietary glucose could become limiting in
the exercising rat dam even if food intake were adequate or increased.
As a further explanation, we noted that chronic, mild exercise and
restricted dietary glucose (20 vs. 60% glucose) independently lowered
concentrations of maternal liver glycogen on Ld 15, indicating that
maternal glucose homeostasis had been compromised under these
diet-exercise conditions. These results showed that imposing
exercise on lactating rats with compromised liver glycogen reserves may
create a competition for glucose that results in lower milk lactose
production rather than reduced glucose supply to exercising muscle; our
maternal plantaris and soleus muscle glycogen concentrations were
comparable among all of the dietary and exercise groups. Whether these
same results would be observed in trained rats in which liver glycogen
may not be decreased (Mottola and Christopher 1991
,
Mottola et al. 1993
) would require further study.
Of the major milk macronutrients, milk protein is generally thought to
be relatively unaffected by changes in glucose-lipid (Koski et al. 1990
, Koski and Hill, 1990
, Lanoue and Koski, 1994
, Romsos et al. 1981
,
Treadway and Lederman, 1986
) and even protein content of
the maternal diet. However, we and several other researchers have
reported surprising increases in milk protein levels after exercise
(Dewey et al. 1994
, Lamb et al. 1979 and 1981
). In our study, we observed an interaction between dietary
glucose level and low intensity exercise that led to significantly
higher milk protein concentrations in exercised compared with rested
dams fed the 40% (vs. 60%) glucose diet. These same high levels were
maintained when the maternal dietary glucose was further restricted to
20%, but in this last-mentioned case, both the exercised and
rested dams had equally high levels. The biological significance of
this increase in milk protein is unclear, but it has been suggested
that it may provide a biological adaptation to maintaining energy
density when milk volume is decreased (Lamb et al. 1979 and 1981
). However, because volume changes were not observed in our
rat study or the human study by Dewey et al. (1994)
, it
would appear that this biological adaptation, which is beneficial to
the nursing offspring, may follow exercise or inadequate carbohydrate
intake and may not require volume changes as had been suggested by
Lamb et al. (1979 and 1981)
.
The requirement suggested by the NRC (1978
, and 1995)
for metabolizable energy for a pregnant or lactating rat calls for
>60% dietary carbohydrate; however, in this study, significantly
heavier pup weights were achieved with a 40% glucose, 22% fat diet
(moderate level of carbohydrate and fat) compared with a 60% glucose
diet (14% fat), thus bringing into question the appropriateness of
this recommendation. Daily milk energy per pup and milk fat per pup
increased significantly from the 20 to the 60% glucose diet groups
(data not shown), but the apparent higher energy intake driven by
increased milk fat was not transferred to increased pup body weight.
Whether increased energy expenditure or some other mechanism fueled
these differences is not clear from this study; however, we can suggest
the possibility that milk composition plays a more important role in
offspring growth than previously thought. A significant positive
correlation between milk fat concentration and weight gain of rat pups
was found in the first but not in the second 10 d of life
(Mozes et al. 1993
). It is also possible that growing
pups may not be able to tolerate high concentrations of milk fat, which
was the macronutrient most increased in the 60% glucose diet, because
the intestinal phase of fat digestion is incomplete due to low
pancreatic lipase activity and bile salt levels (Hamosh et al. 1994
). It remains to be seen whether our weight difference
would be sustained beyond Ld 15 and whether heavier is necessarily
healthier; however, our results indicate that, at least in
litter-bearing rats, a maternal diet with lower carbohydrate (40%
glucose) and higher fat (22%) may better promote pup growth up to Ld
15. In support of this, Guo and Jen (1995)
found that
weanling rat pups (22 d old) from dams that were fed a 40% fat, 30%
carbohydrate diet were significantly heavier than weanlings of dams fed
a control diet of 4.5% fat.
In summary, our results showed that during pregnancy, restricted
maternal dietary glucose and mild chronic exercise did not compromise
postnatal survival, but during lactation, decreased availability of
dietary glucose and fat and mild or low intensity chronic exercise did
indeed alter lactation performance. We observed that low intensity
chronic exercise increased milk fat concentrations, which may have been
fueled by mobilization of mammary gland fat reserves. Our results also
showed that maternal dietary glucose intake from 20 to 60% produced
graded levels of milk fat, and that a moderate carbohydrate (40%
glucose), moderate fat diet may be more appropriate for increased pup
growth. We suggested that the requirements indicated by the NRC
(1978
and 1995)
for carbohydrate in the lactating rat may be
too high for optimum lactation performance and that a more moderate
level of maternal dietary carbohydrate and higher level of dietary fat
than what is traditionally fed to lactating dams may be more
appropriate for pup growth.
Implications of our findings for humans may be limited, given that the
proportion of total energy required for lactation in rats is much
greater than that in humans. However, because mammary gland physiology
is similar across species, biological concepts developed from the
lactating rat model may be instructive for human lactation. Data from
this study suggest that the increase in milk fat with mild exercise may
be mediated by increased mammary gland fat mobilization. In support of
increased fat mobilization in exercising humans, Dewey (1998)
has suggested that when dietary intake is controlled,
high level aerobic activity during lactation in women enhances body
lipid mobilization and protects milk energy output. Dewey (1998)
also reported that leaner women who dieted were more
likely to have decreased milk energy outputs than heavier women who
dieted. We speculate that if women reduce fat or carbohydrate intake
and increase exercise in an attempt to lose weight, lactation
performance may suffer. Indeed, Paul et al (1979)
,
supported by circumstantial evidence, suggested that dietary intake
during pregnancy is critical to lactation performance due to the
accretion of body fat stores. In the developing world, body fat is low,
physical activity is high (Institute of Medicine 1990
)
and diets are high in carbohydrate and low in fat (Perisse et al. 1969
). The idea suggested by our study that a more moderate
carbohydrate, higher fat intake may be required for optimum lactation
could have implications in the developing world and warrants further
investigation.
|
FOOTNOTES |
|---|
2 A.Y.M. and K.L.E. were recipients of graduate
student scholarships from the Fonds pour la Formation de Chercheurs et
l'Aide du Québec (FCAR), a Québec provincial funding
agency.
4 Abbreviations used: E, chronically exercised;
Gd, gestation day; Ld, lactation day; R, rested.
5 Total work expended was calculated with the
following formula: work in kg·m = [(% grade) x (m/min) x
(durationmin) x (body masskg)].
Manuscript received June 24, 1998. Initial review completed August 31, 1998. Revision accepted February 24, 1999.
|
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20% GLUC different from 60% GLUC,
P < 0.05.
