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Department of Animal Science and North Carolina Institute of Nutrition, North Carolina State University, Raleigh, NC 27603 and * Department of Food Science and Human Nutrition and Division of Nutritional Sciences, University of Illinois, Urbana, IL 61801
3To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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3), dietary fat (0 vs. 10%), and
farrowing (natural vs. induction via lutalyse on d 112). Piglets
suckling fat-supplemented dams grew up to 25% faster than control
pigs nursing unsupplemented sows (250 vs. 200 g/d; P
< 0.01). Improved growth was correlated with elevated milk fat
and insulin-like growth factor (IGF) concentrations associated with
fat supplementation. Dietary fat elevated milk fat concentration at 48
and 72 h postfarrowing by 21.6 and 22.6%, respectively
(P < 0.05). Compared with nonfat-fed controls,
multiparous sows fed 10% fat showed a more consistent rise in milk fat
concentration, with 26% and 41% elevations for induced or naturally
farrowing sows, respectively, vs. a 19% reduction or a 1% elevation
in induced or naturally farrowing gilts (P < 0.01). The concentration of milk IGF-I tended to be lower in gilts
than in multiparous sows (P < 0.2, 95.7 vs. 117.4
µg/L), and levels were particularly low in milk from
induced gilts receiving no additional dietary fat (44.7
µg/L). However, fat supplementation elevated IGF-I
to levels (110.6 µg/L) exceeding those measured in
unsupplemented, naturally farrowing control sows and gilts (95.8
µg/L). In conclusion, supplemental dietary fat
elevates milk fat in multiparous sows more than primiparous gilts
regardless of farrowing treatment (induced vs. natural farrowing) and
improves piglet growth throughout lactation irrespective of parity or
farrowing treatment. The potential of supplemental dietary fat to
reverse the reductions in milk IGF-I observed in first-parity
females and in dams induced to farrow merits further
investigation.
KEY WORDS: • dietary fat • insulin-like growth factor • milk composition • swine • lactation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). With
the additional knowledge that piglets are born with as little as 2% of
body weight as fat (Curtis et al. 1966
, Friend 1974
, Seerley et al. 1974
) and that reserves of
stored glycogen also are limited (Boyd et al. 1978
), the
importance of rapid and adequate colostrum intake by the newborn pig is
clear (Noblet et al. 1997
). In addition, the widespread
adoption of segregated early-weaning strategies to reduce disease
transfer from mother to offspring involves the weaning of piglets as
early as 10–14 d of age. The success of this management technique is
dependent on rapid piglet growth during the brief suckling period. But
what can be done to enhance early postnatal growth?
Increasing the fat content in colostrum may increase the energy supply
to newborn piglets, thereby improving survival (Pettigrew 1981
) and perhaps growth rate. The fatty acid profile and
amount of milk fat can be manipulated by the source of dietary fat
provided to the dam both in late gestation and throughout lactation
(Jackson et al. 1995
, Seerley et al. 1974
). Further enhancement of neonatal tissue development may
occur when piglets consume colostrum high in growth factors such as
insulin-like growth factor
(IGF)4
-I and -II due to their mitogenic potential (Burrin et al. 1997
, Houle et al. 1997
, Odle et al. 1996
). Because milk composition is linked to mammary
development (Kensinger et al. 1986
), primiparous sows
may secrete milk lower in energy and/or growth factor content. In
addition, milk from dams induced to farrow early may contain less milk
fat because considerable lipid secretion does not occur until
parturition is imminent (Jackson et al. 1995
,
Kensinger et al. 1986
). We hypothesized that
supplemental dietary fat would correct the putative reduction in milk
fat and/or growth factor content associated with induced farrowing,
especially in primiparous dams. Thus our objectives were to examine
interactions among dietary fat (0 vs. 10%), parity (gilts vs. parity
3) and farrowing (natural vs. induced) treatments, and their
effects on milk composition as well as sow and litter performance.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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3) (Pig Improvement Co., lines 231/233) were selected
from the swine farm of the Lake-Wheeler Field Laboratory (North
Carolina State University, Raleigh, NC) and randomly assigned to one of
four treatment groups according to a 2 x 2 x 2 factorial
design. Treatments included diet (0 vs. 10% choice white grease),
parity and farrowing (natural vs. induced on d 112) variables. The
dietary treatments were initiated on d 90 of gestation and were
continued throughout the 21-d lactation period. From d 90 of gestation
until farrowing, dams received 2 kg daily of their respective gestation
diets (Table 1
). The NRC (1988)
recommends that gestation
diets contain 12% crude protein (CP), 0.43% lysine and 13431 kJ (3210
kcal) metabolizable energy (ME)/kg. For gestation, diets were
formulated to contain 17% more CP and 55% more lysine than NRC (1988)
recommendations. Energy content of the gestation and lactation diets in
our study were similar. The control diet provided 13.828 MJ (3305 kcal)
ME/kg and the fat-supplemented diet provided 15.652 MJ (3741 kcal)
ME/kg, exceeding the NRC requirement by either 3 or 16.5%,
respectively. On d 109, dams were moved into crates in the farrowing
house. After farrowing, lactation diets were consumed by dams ad
libitum (Table 1)
. Lactation diets exceeded NRC (1988)
recommendations for CP (13%) and lysine (0.60%) by 18.8 and 34.2%,
respectively. Dams had free access to water.
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(PGF2, Upjohn, Kalamazoo, MI) on d
112. Induced sows farrowed within 24–36 h of injection. Average
gestation length for induced pigs was 114 d, whereas gestation
length for naturally farrowing pigs averaged 116 d.
Mammary secretions were collected from the right first thoracic gland
beginning at the birth of the first pig (0 h) and subsequently at 3, 6,
9, 12, 24, 48, 72 and 168 h postpartum. Pigs were denied access to
the right first thoracic gland for the first four sampling times.
Samples were collected by hand stripping of the gland for 0 through
6 h, when there was free flow of colostrum. For subsequent
sampling times, 0.5 mL of oxytocin (20,000 USP units/L, Anpro
Pharmaceutical, Arcadia, CA) was administered intramuscularly to
facilitate milk letdown. Samples were stored at -20°C until they
were analyzed for total protein (Lowry et al. 1951
; BSA
standard), lactose (Teles et al. 1978
), fat (Babcock
method; AOAC 1984
), and IGF-I and -II
(Donovan et al. 1994
). The protein and lactose
colorimetric assays were run in triplicate (average CV 
4%),
and standard curves were linear (r2 0.995). Babcock fat analyses were performed in duplicate, using 8%
bottles. Milk IGF-I and -II concentrations were measured by
specific RIA as previously described (Donovan et al. 1994
). Before assay, IGF binding proteins were extracted by
acid gel filtration chromatography (Donovan et al. 1994
). Dilution factors used in the IGF-I assay were as
follows: for 0-, 6- and 12-h samples, 1:40 to 1:60; for the 24-h
samples, 1:30; and for the 48-h samples, 1:5. Interassay and
intra-assay coefficients of variation for the IGF-I assay were
2 and 7%, respectively. Dilution factors used in the IGF-II assay
were as follows: for 0-, 6- and 12-h samples, 1:30 to 1:40; for the
24-h samples, 1:15; and for the 48-h samples, 1:10. Interassay and
intra-assay coefficients of variation for the IGF-II assay were
8 and 6%, respectively.
Dam weights were recorded on d 90, d 109, at farrowing and at weaning. Dam feed intake was recorded daily during lactation. Piglets born alive, stillborns and mummies were recorded on d 1 of lactation. Piglets were weighed at birth, d 7 and 14 and at weaning (mean, 21 d). Dams were required to nurse 7–12 piglets to remain in the study. When females farrowed > 12 piglets, extra piglets (beyond 12) were randomly selected and removed within 48 h postfarrowing. If a dam with < 7 piglets farrowed within 24 h of a dam receiving the same treatment who had > 12 pigs, 1–2 piglets were cross-fostered so that the dam did not have to be removed from the experiment. No cross-fostering was applied to any litter after 48 h when the number of piglets on each sow was recorded to determine survival (%) from 48 h to d 21.
Statistical analysis.
Performance data were analyzed using the GLM procedure of the
Statistical Analysis System (SAS 1985
) appropriate for a
2 x 2 x 2 factorial, randomized complete block design. Milk
composition data were modeled according to a split-plot in time
(Steel and Torrie 1980
) appropriate for a factorial
experiment. The whole-plot error (error A) was used to evaluate the
significance of the main-plot effects (fat, parity and induction
variables), and the residual error term was used to test the
significance of the time effect and the interactions between
main-plot and time effects. Effects with P 0.1 are considered meaningful, and P 0.05 is
significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Overall, performance data (Table 2
) were similar, in general, to values reported by others (Coffey et al. 1994
, Seerley et al. 1981
, Shurson et al. 1986
, Tilton et al. 1999
). Feed
consumption during lactation was not affected by parity or dietary fat
and averaged 4.54 kg/d for all eight treatments. Lactation feed intake
tended to be higher (13%) in dams allowed to farrow naturally compared
with dams given PGF2 on d 112 (4.82 vs. 4.27
kg/d; P < 0.07). To our knowledge, feed intake has not
been reported for induced dams compared with that of naturally
farrowing dams. Increased respiration rate and increased nervousness
were signs observed in dams receiving an infusion of
PGF2 (Diehl et al. 1974
); these behaviors also are associated with sick
animals who tend to reduce their feed intake (O’Grady et al. 1985
). Primiparous dams gained more (10.9 ± 1.5
kg) than multiparous dams (3.6 ± 1.4 kg) during gestation (d
90–109; P 0.01). However, treatment effects on
weight loss at parturition and during lactation were not detected
(P > 0.10).
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; however, gilts farrowed 9.75 ± 0.5 live piglets, which was 19% less than (P < 0.01) the number born to multiparous sows (11.98 ± 0.5). The
number of stillborn pigs was correspondingly affected by parity, with
0.29 ± 0.23 stillborns per litter for gilts and 1.35 ± 0.23
for sows (P < 0.01). Diet also affected
stillbirths with 0.48 ± 0.23 for dams consuming the nonfat
control diet compared with 1.17 ± 0.23 for dams consuming the
diet with 10% supplemental fat (P < 0.04).
Induction of farrowing with prostaglandin resulted in a >twofold
elevation in stillbirths, with 0.42 for naturally farrowing dams
compared with 1.23 for dams induced to farrow on d 112
(P < 0.02). An 82% reduction in the number of
mummies was observed in gilts compared with multiparous sows (0.08 vs.
0.49 mummies/litter; P < 0.03), but no effects of
diet or farrowing induction were observed.
Piglet average daily gains over each week of lactation (data not shown)
and over the entire lactation interval (Table 2)
were increased by up
to 25% when dams were fed supplemental dietary fat (P
< 0.01). Total litter weaning weight was elevated by 14% in dams
fed 10% dietary fat (P < 0.06, data not shown),
despite a reduced number of pigs weaned compared with the nonfat
control group (P < 0.05). Piglets nursing
multiparous sows gained 9% faster than those nursing first-parity
gilts (P < 0.01). Similarly, pigs suckling dams
that farrowed naturally grew 30% faster than pigs nursing dams that
were induced to farrow (P < 0.01). Survival from
48 h to weaning was 20.6% higher in gilts than in sows (94.7
± 3.7 vs. 78.5 ± 3.6; P < 0.01).
Heavier breeding weights and higher parity have been associated with
increased piglet mortality (Newton and Mahan 1993
).
Milk composition.
Milk fat concentrations were relatively low and constant (~6%)
during the first 9 h postfarrowing and then increased
significantly at 12 h and thereafter (time main effect,
P < 0.01), peaking at 48–72 h particularly in the
fat-supplemented dams (Fig. 1A
; fat x time, P < 0.01). Indeed, milk fat
concentration was 22% higher at 2–3 d postfarrowing in dams fed
supplemental fat. Furthermore, the effect of supplemental fat was
influenced by parity and by induction of farrowing (fat x parity
x induction, P < 0.01; Fig. 1B
). When
supplemental fat was fed to mulitiparous sows, regardless of
prostaglandin treatment, a more consistent positive response was
observed in milk fat concentration compared with first-parity
gilts. That is, milk fat concentration of sows was elevated by
supplemental fat regardless of whether they were induced or farrowed
naturally, whereas dietary fat had no effect on naturally farrowing
gilts and tended to reduce milk fat percentage in induced gilts.
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Milk IGF-I and IGF-II concentrations decreased by 93 and 76%,
respectively, over the first 48 h postfarrowing (Table 3
, P < 0.01). At all sampling times, concentrations of
IGF-I were numerically higher in colostrum of fat-fed dams than
in unsupplemented controls, but differences were greater over the first
12 h (fat x time interaction, P < 0.1). In
general, concentrations of IGF-I were lowest in milk from induced
dams receiving no supplemental fat and highest in naturally farrowing
dams fed supplemental fat, with other treatments intermediate
(Fig. 2A
; fat x induction x time, P < 0.05).
Overall, milk IGF-I concentration in gilts was numerically lower
than in sows (95.7 ± 11.8 vs. 117.4 ± 13.9
µg/L, P < 0.2), but was particularly low
(44.7 µg/L) in induced gilts fed no supplemental fat (Fig. 2B
). Fat supplementation of induced gilts elevated IGF-I
to concentrations exceeding the unsupplemented, naturally farrowing
sows and gilts (Fig. 2B
; fat x parity x induction, P < 0.1). However, average IGF-I
concentrations reached the highest levels in naturally farrowing,
fat-supplemented sows and gilts.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Effects on milk nutrients.
The importance of feed (energy) intake in reproducing
females, especially during late gestation and lactation, and its direct
effect on fetal and neonatal growth and development is unequivocal. If
diets do not adequately provide for the maintenance and production
needs of modern high lean genotype sows, then energy provided to the
litter is reduced and performance suffers (Pettigrew et al. 1993
). Indeed, because piglet endogenous energy stores are
limited at birth, sufficient milk energy intake during the first
72 h after birth is imperative to ensure survival. Inadequate
supply of exogenous nutrients weakens the piglet, making it more
susceptible to death from other factors such as crushing, disease and
hypothermia (USDA 1997
). Therefore, increasing the
energy content of colostrum could improve neonatal survival and growth.
We showed previously (Jackson et al. 1995
) that dietary
fat could abrogate reductions in milk fat concentration of sows induced
to farrow prematurely (d 110–115). This study was designed to expand
on these findings by comparing effects in first-parity gilts to
multiparous sows.
Considering the potential impact on mammary development of gilts,
Weldon et al. (1991)
studied the effects of increased
dietary energy during 75–90 d of gestation on mammary development and
found that the mammary parenchymal weight and DNA content were
significantly lower in gilts fed the excess energy. They concluded that
the increase in energy was detrimental to secretory tissue development.
Thus, the timing of dietary fat supplementation to the dams is an
important consideration. Histology studies by Kensinger et al. (1982
and 1986)
indicate that the growth of the
mammary tissue is complete by d 90, and the differentiation of alveolar
epithelial cells begins subsequently. This marks the beginning of
lactogenesis, and no further negative effects of supplemental dietary
energy have been found after this time. Furthermore, d 90 marks the
point at which small lipid droplets are visible in the basal portion of
the differentiating epithelial cell (Kensinger et al. 1986
). Therefore, if increased energy is added to the diet in
lipid form, it may be most beneficial to begin feeding supplementation
after d 90 of gestation. Because epithelial cell differentiation does
not appear to be complete until d 4 of lactation (Kensinger et al. 1986
), we hypothesized that premature parturition
(especially in gilts) may have a detrimental effect on the fat content
of secretions expressed during the second stage of lactogenesis.
However, this was not observed. Among the control dams not supplemented
with dietary fat, induction of farrowing increased milk fat
concentration compared with naturally farrowing dams, without regard to
parity. In contrast, the milk fat content of sows could be increased
further by dietary fat supplementation, but gilts failed to respond.
Although many others have shown that dietary fat supplementation
increases sow’s milk fat (Boyd et al. 1978
,
Jackson et al. 1995
, Pettigrew 1981
,
Seerley et al. 1974
, Stahly et al. 1981
),
the reason that first-parity gilts failed to respond remains
unclear; it may be due to the variability in mammary development and
body energy reserves of gilts compared with multiparous sows. De novo
fatty acid synthesis by the gilt mammary gland may not be as well
developed; when metabolic signals such as insulin/glucagon are
influenced by the ratio of energy supplied by dietary fat and
carbohydrate, then a reduction in milk fat may occur. As a proportion
of body fat at farrowing, fat loss during lactation in parity 1 and 2
sows was greater (P < 0.04) than fat loss in older
(parity 3) sows (Clowes et al. 1994
).
Alternatively, because an energy dependency exists for milk production
(Tokach et al. 1992
), the amount of energy consumed can
change the amino acid demand for milk synthesis. The lysine to energy
ratio of the diets used in this study were not constant, and increased
protein may benefit the gilt because the growth rate of lean tissue is
high in young dams (Whittemore and Yang 1989
).
The milk protein and lactose concentrations (data not shown) followed
the pattern (decreasing and increasing, respectively) previously
reported (Jackson et al. 1995
). Additionally, no
treatment differences were noted in either study. Research by
Shurson et al. (1986)
also failed to detect differences
in milk protein when 10% dietary fat was fed to sows. If there are no
changes in protein or lactose levels and the milk fat concentration
increases (as observed), the percentage of energy per gram of milk
provided by the protein or lactose will decrease. This should not alter
the volume of colostrum or milk consumed by the piglet because they do
not appear to regulate intake according to the energy density of the
milk (Le Dividich et al. 1997
). Because piglet milk
intake was not affected by milk fat concentration, a 31.5% increase in
ME was measured (LeDividich et al. 1997
). Because low
birth weight is associated with increased mortality, provision of extra
energy by an increase in colostral and milk fat levels when sow diets
are supplemented with fat may have a positive influence on survival
(Cieslak et al. 1983
). Other benefits produced include
the increase in preweaning gain. A 25% increase in average daily gain
in piglets suckling sows fed fat and an overall 14% increase in litter
gain in fat-supplemented dams were observed in this study.
Supplemental fat has been shown to increase the volume of milk produced
by the sow as much as 33.6% (Coffey et al. 1982
).
However, this may be of less relative importance because Atwood and Hartmann (1992)
noted a higher correlation between piglet
weight and the amount of ingested fat than the volume of milk intake.
In summary, induction of premature parturition did not result in milk
fat depression as reported previously (Jackson et al. 1995
), nor were first-parity gilts more susceptible to such
putative effects as originally hypothesized. Multiparous sows, whether
induced or naturally farrowing, responded well to dietary fat
supplementation with increased milk fat concentration.
Effects on milk IGF-I.
IGF-I and -II play several roles during pregnancy and lactation in the
sow. They are intricately involved in mammary gland function in the sow
as well as having some bioactivity in the neonatal gastrointestinal
tract. IGF-I may mediate the actions of growth hormone in the
mammary gland. Growth hormone likely supports synthesis of milk rich in
energy by playing a role in the synthesis of milk fat (Flint 1995
). If increased dietary fatty acids are available, these
hormones could be involved in directing the fatty acids to milk fat
synthesis in the mammary gland. The IGF-I levels at each time point
were greater in dams fed fat compared with those receiving no
additional dietary fat (Table 3
, Fig. 2
). Other roles played by IGF in
the mammary tissue of sows include possible stimulation of mitogenesis
and galactopoiesis (Shamay et al. 1988
).
If circulating levels of IGF-I are elevated in the sow, this would
likely lead to elevated levels in the colostrum and milk because serum
appears to be the main source of milk IGF-I (Donovan et al. 1994
). The mammary gland has very low levels of IGF-I mRNA
and would not be the primary source of IGF-I in the milk
(Tavakkol et al. 1988
). This is likely the case for milk
IGF-II as well. The ratio of IGF-I and -II levels measured in
our study was not consistent with that in the previous experiment by
Donovan et al. (1994)
. Breed can influence IGF-I and
-II concentrations within a species (Baumrucker and Blum, 1993
). If serum IGF concentrations vary with genotype,
and the ratio of serum IGF-I and IGF-II was different in the
pigs used in this study, the milk IGF-I and -II levels may have
reflected this difference. Furthermore, dietary fat was not increased
in those studies, and it may have influenced the serum IGF-I and
-II concentrations. Unfortunately, blood samples were not collected
from the dams in this experiment.
The effects of these growth factors on piglet intestinal and
whole-body growth have been studied by several researchers
(Baumrucker and Blum 1993
, Burrin et al. 1992
and 1996
, Donovan and Odle 1994
, Donovan et al. 1996
). The growth factor peptides in colostrum appear to
pass unharmed (in part) through the stomach as a result of lower
secretion of gastric acid and then bind to their receptors in the small
intestine without breakdown by enzymes because of the immaturity of the
neonatal gut (Lebenthal et al. 1983
). Once IGF-I and
-II reach the intestine, they may elicit a response in the intestinal
epithelium (Burrin et al. 1996
, Donovan et al. 1996
). Indeed, supplementation of formula with IGF-I has
been shown to increase small intestinal mass and villous height as well
as lactase and sucrase activity (Burrin et al. 1996
,
Houle et al. 1997
). If IGF-I and -II exert
immunological effects on the gut (Baumrucker and Blum 1993
) or speed intestinal repair after infection (Odle et al. 1996
), it might prove beneficial to increase the levels
of these growth factors in sow colostrum and milk via prophylactic or
transgenic approaches.
In conclusion, supplemental dietary fat in sow diets can elevate milk fat concentration, especially 2–3 d postpartum, regardless of parity or parturition treatment. The increase in milk fat when dietary fat was added was more consistent in multiparous sows than in gilts. An increase in milk fat will increase the energy available to the piglet and has the potential to affect postnatal survival and growth. Indeed, piglet growth rate was improved by 25% over a 3-wk lactation period. Induction of farrowing did attenuate IGF-I concentrations in milk; however, this depression was abrogated with supplemental dietary fat. This may be of importance because the IGF may stimulate digestive enzyme activity in the neonatal intestinal epithelium and thus lead to improved nutrient assimilation. Collectively, working through elevated milk fat and/or IGF-I and -II, supplemental dietary fat appears to accelerate the growth of suckling piglets without regard to the parity of the dam (gilt vs. sow) or farrowing status (induced vs. naturally farrowing).
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FOOTNOTES |
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2 Supported in part by the Fats and Proteins Research Foundation, and by the North Carolina Agricultural Research Service.
4 Abbreviations used: CP, crude protein; IGF, insulin-like growth factor; ME, metabolizable energy;
PGF2, prostaglandin F2.
Manuscript received March 17, 1999. Initial review completed April 14, 1999. Revision accepted August 4, 1999.
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