J. Anim. Sci. 2002. 80:3286-3300
© 2002 American Society of Animal Science
Protein (lysine) restriction in primiparous lactating sows: Effects on metabolic state, somatotropic axis, and reproductive performance after weaning1
C. A. Mejia-Guadarrama2,
A. Pasquier,
J. Y. Dourmad,
A. Prunier and
H. Quesnel3
Unité Mixte de Recherches sur le Veau et le Porc, INRA, 35590 Saint-Gilles, France
3 Correspondence:
Phone: +33 2 2348 56 49; fax: +33 2 2348 50 80; E-mail:
quesnel{at}st-gilles.rennes.inra.fr.
 |
Abstract
|
|---|
Low protein intake during lactation has been demonstrated to increase the loss of body protein and to reduce the reproductive performance of female pigs. The objectives of the current experiment were 1) to determine whether protein (lysine) restriction alters levels of somatotropic hormones, insulin, follicle-stimulating hormone, and leptin around weaning, and 2) to evaluate the relationships between these eventual alterations and postweaning reproductive performance. One day after farrowing, crossbred primiparous sows were randomly allocated to one of two diets containing 20% crude protein and 1.08% lysine (C, n = 12) or 10% crude protein and 0.50% lysine (L, n = 14) during a 28-d lactation. Diets provided similar amounts of metabolizable energy (3.1 Mcal/kg). Feed allowance was restricted to 4.2 kg/d throughout lactation, and litter size was standardized to 10 per sow within 5 d after farrowing. Catheters were fitted in the jugular vein of 21 sows around d 22 of lactation. Serial blood samples were collected 1 d before (day W - 1) and 1 d after (day W + 1) weaning, and single blood samples were collected daily from weaning until d 6 postweaning (day W + 6). Sows were monitored for estrus and inseminated. They were slaughtered at d 30 of gestation. During lactation, litter weight gain was similar among treatment groups. Reduced protein intake increased (P < 0.001) sow weight loss (-30 vs -19 kg) and estimated protein mobilization throughout lactation (-4.1 vs -2.0 kg). On day W - 1, L sows had higher (P < 0.02) plasma glutamine and alanine concentrations, but lower (P < 0.05) plasma tryptophan and urea than C sows. Mean and basal plasma GH were higher (P < 0.001), whereas plasma IGF-I and mean insulin were lower in L than in C sows on day W - 1. Preprandial leptin did not differ between treatments on day W - 1, but was higher (P < 0.01) in L sows than in C sows on day W + 1. Mean FSH concentrations were similar in both treatments on day W - 1 (1.3 ng/mL), but L sows had greater (P < 0.001) mean FSH on day W + 1 than C sows (1.6 vs 1.2 ng/mL). The weaning-to-estrus interval (5 ± 1 d) was similar in both groups. Ovulation rate was lower in L than in C sows (20.0 ± 1 vs 23.4 ± 1, P < 0.05). No obvious relationships between reproductive traits and metabolic hormone data were observed. In conclusion, these results provide evidence that protein (lysine) restriction throughout lactation alters circulating concentrations of somatotropic hormones and insulin at the end of lactation and has a negative impact on postweaning ovulation rate.
Key Words: Insulin-Like Growth Factor • Lactation • Metabolism • Protein Intake • Reproduction • Sows
|
Introduction
|
|---|
During lactation, voluntary feed intake of highly prolific sows is frequently inadequate to meet nutrient requirements for maintenance and milk yield, and these sows must mobilize fat and protein reserves (O’Grady et al., 1985; Noblet et al., 1990). Low protein intake during lactation has been demonstrated to increase body protein loss (Jones and Stahly, 1999a) and reduce reproductive performance (King and Williams, 1984a; Brendemuhl et al., 1987; Yang et al., 2000a,b). There is increasing evidence that nutrition and changes in metabolic state influence the reproductive axis through variations in metabolites and associated metabolic hormones, including insulin, IGF-I, GH, and leptin (for review, see Schams et al., 1999; Prunier and Quesnel, 2000). However, much emphasis has been given to insulin and IGF-I, and less attention has been paid to GH. It is widely accepted that insulin and somatotropic hormones (GH and IGF-I) play a key role in the regulation of fat and protein metabolism in the sow, as in other species (Breier, 1999). The aim of the present experiment was to test the following hypotheses: 1) low protein intake in sows induces alterations in somatotropic hormones and insulin, and 2) such alterations are associated with changes in postweaning reproductive performance of primiparous sows.
|
Materials and Methods
|
|---|
Animals and Experimental Design
The experiment was conducted in four replicates on a total of 29 Pietrain x (Large White x Landrace) crossbred gilts. They were inseminated at 270 ± 8 d of age and 180 ± 3 kg live weight. Throughout the experiment, females were maintained under artificial light provided by incandescent lamps. Light duration decreased from 12 to 10 h/d between d 42 and 84 of gestation and remained constant thereafter (10 h/d). Gilts were moved from the gestation to the farrowing rooms on d 104 ± 1 of gestation and were kept in individual farrowing crates (2 x 2.5 m) in a building maintained between 20 and 25°C. When necessary, parturition was induced by an i.m. injection of 2 mL of cloprostenol (Planate, Mallinckrodt Veterinary, Meaux, France) on d 114 of gestation. Farrowing occurred on d 114 or 115 of gestation. Within 48 h after birth, litters were standardized to 11 piglets, and to 10 piglets 3 d after. Piglets that died were weighed and replaced by piglets of similar weight and age. They had no access to creep feed. Throughout lactation, piglets had free access to the dam. They were weaned between 0830 and 0930 at 28 ± 1 d of age (W). Water was freely available for the sows and the piglets throughout the experimental period.
During gestation, all females were fed a diet containing 2.9 Mcal of ME/kg, 13% CP, and 0.6% lysine once daily (around 0830). This feed allowance was calculated to meet 110% (about 2.7 kg of feed/d) of the energy requirements for gestation (NRC, 1988). On the day of farrowing (d 0), all females were allowed to consume 1 kg of the gestation diet. During lactation, the daily feed allowance was given in two equal meals provided around 0830 and 1430. One day after farrowing, lactating primiparous sows were randomly assigned within replicate to either a control (C: 20% CP and 1.08% lysine) or a low- (L: 10% CP and 0.5% lysine) protein diet (Table 1
). The L and C diets were formulated on the basis of lysine being the first-limiting AA with other AAs meeting or exceeding the suggested "ideal" ratio of each AA relative to lysine for lactating sows (INRA, 1989). Diets provided similar amounts of ME (3.1 Mcal/kg; Table 1). On d 1, 2, and 3 postpartum, all females received 2.5, 3.5, and 4.5 kg/d of the experimental diet, respectively. Thereafter, the amount of feed was restricted to 4.5 kg/d of the experimental diets throughout lactation to prevent differences in feed consumption. Feed refusals were weighed daily before the morning meal and actual feed intake was then calculated. From day W until the end of the experiment, all sows received 2.5 kg/d of a conventional gestating sow diet containing 2.9 Mcal of ME/kg, 13% CP, and 0.6% lysine, in two equal meals given at around 0830 and 1430. At weaning, sows remained in their farrowing crate for 2 d in order to facilitate serial blood sampling. Thereafter, they were moved and penned in individual gestation crates (0.7 x 2.5 m) until the end of the experiment.
Estrus, Ovaries, Ovulation Rate, and Embryonic Survival
From 2 d after weaning (day W + 2), sows were monitored for estrus twice daily at 0800 and 1600 by exposing them to fenceline contact with a mature boar for 15 min and using the back-pressure test. Sows were artificially inseminated twice with fresh diluted semen from Pietrain boars. When first observation of standing estrus occurred in the morning, first insemination was performed 8 h later, whereas insemination was performed 16 h later when estrus was first detected in the afternoon. The second insemination was performed 24 h after the beginning of estrus in both cases. Doses of semen (3 x 109 spermatozoa/70 mL) consisted of pooled semen. The same pool was used for all sows belonging to a same replicate. Sows were slaughtered at the local abattoir 30 ± 1 d after insemination and the genital tract was immediately collected after death. Weights of the two ovaries were recorded. All corpora lutea were dissected and counted. To collect embryos, the wall of uterine horns was cut longitudinally, starting at the uterocervical junction. The number of live or dead embryos was recorded. An embryo was considered dead on the basis of size visual evaluation (clearly less than the mean for all embryos from that sow) and/or by the observation of a necrotic process in situ. Embryo survival was expressed as the percentage of corpora lutea represented by live embryos.
Measurements and Sampling
Piglets were weighed at birth and at 7, 14, 21, and 28 ± 1 d of age. Sows were weighed 1 d after farrowing and at 7, 14, 21, and 28 ± 1 d postpartum. On the same day, sow backfat thickness was ultrasonically measured (Sonolayer SAL-32B, Toshiba, Tokyo, Japan) at 65 mm on each side of the dorsal midline at the level of last rib (P2).
A subgroup of sows was randomly allocated to intensive blood sampling (C, n = 10; L, n = 11). On d 22 ± 1 of lactation, an indwelling Silastic (Dow Corning, Midland, MI) catheter was surgically inserted into the right jugular vein of the sows while they were under general anesthesia, as previously described (Camous et al., 1985). Sows were deprived of feed 16 h before the surgery. Around 1 h after surgery, sows returned to their farrowing crate and were immediately re-fed. Housing and feeding were previously described. However, feeding troughs were emptied, when necessary, at around 1600 on the day before serial blood sampling. Serial samples were collected via catheter every 15 min from 0815 to 1615 on the day before (day W - 1) and on the day after (day W + 1) weaning. Additionally, single blood samples for IGF-I were taken at 1400 on day W and from day W + 2 to day W + 6. Blood samples were collected in heparinized tubes, immediately placed on ice, and centrifuged within 15 min for separation of plasma. Plasma samples were stored at -20°C until assay.
Analyses
Hormone Assays.
Plasma concentrations of insulin, GH, IGF-I, and FSH were determined in duplicate using validated RIA (Louveau et al., 1991; Louveau and Bonneau, 1996; and Camous et al., 1985, respectively). Leptin concentrations were determined with a multispecies double-antibody kit assay (Linco Research Inc., St. Louis, MO), which was previously validated in the porcine species (Qian et al., 1999). Samples were run in two assays for insulin and IGF-I, and in a single assay for GH, FSH, and leptin. Insulin and GH concentrations were measured every 15 min, and FSH was measured every hour from 0815 to 1615. Concentrations of IGF-I were analyzed only once a day (at 1400) because of the relatively low variation in IGF-I level throughout the day (Schams et al., 1994). Leptin concentrations were measured once a day before the morning meal (at 0815) in order to focus on fasted levels.
For insulin, the intra- and interassay CV were 7.1% and 11.5% at 40 µIU/mL, respectively, and the average sensitivity of assay, defined as 90% of total binding, was 3 µIU/mL. For GH, the intraassay CV was 15.3% at 2.5 ng/mL, and the average sensitivity was 0.75 ng/mL. Plasma IGF-I concentrations were determined after an acid-ethanol extraction. This extraction technique was validated for plasma samples from lactating and weaned sows (Louveau and Bonneau, 1996). The recovery efficiency was 92%; therefore, sample concentrations were not corrected for recovery. The intra- and interassay CV were 7.4% and 17% at 258 ng/mL, respectively, and the average sensitivity was 7.5 ng/mL. The relative levels of IGFBP on days W - 1 and W + 1 (1400) were quantified using SDS-PAGE, transfer to a nitrocellulose membrane, and incubation in the presence of 125I-IGF-I (Hossenlopp et al., 1986). The relative level of IGFBP was analyzed by densitometric scanning of membranes using phosphorImager (STORM) and Imagequant software (Molecular Dynamics, Bondoufle, France). To prevent gel-to-gel variation in IGFBP evaluation, treatments and days of sampling were represented on each gel. For FSH, the intraassay CV was 5.6% at 1.4 ng/mL, and the average sensitivity was 1.0 ng/mL. The percentage of cross reaction with the porcine leptin was 67% as given by the manufacturer. Results are expressed in human equivalents (HE). The leptin intraassay CV was 5.0% at 4.1 ng HE/mL, and the average sensitivity of assay was 0.9 ng HE/mL.
Metabolite Assays.
Plasma concentrations of glucose, NEFA, and urea were measured on days W - 1 and W + 1, every hour from 0815 to 1615, by automated enzymatic methods (bio-Mérieux kits, ref 61272, Marcy l’Etoile, France; Wako Chemical NEFA C, Neuss Germany, and urea unimate 5, ref.07-3685-6, Roche, Neuilly-sur-Seine, France, respectively) with a Cobas Mira multichannel analyzer (Hoffman-Laroche, Basel, Switzerland). Plasma AA concentrations were measured on day W - 1 at 0815 and 1400, according to the procedure described by Sève et al. (1991). Briefly, plasma was deproteinized with one volume of sulfosalicylic acid (6%) combined with an internal standard (L-
-amino-ß-guanidinopropionic acid). Supernatant fluids were adjusted to pH 2.2 with 100 µL of citric acid (0.5 N) adjusted to pH 5 with lithium hydroxyde (4 N). Chromatographic separation of the AA was performed on a Biotronik LC 5001 analyzer (Biotronic Pusheim Bahnhof, Germany) using a Li+ cation exchange column maintained between 33 and 66°C with postcolumn ninhydrin derivatization. A special run was used to analyze tryptophan. Plasma tryptophan was determined using a sample concentration four times greater than that for the other AA at a column temperature of 75°C, and was quantified using the same chromatographic procedures.
Calculations and Statistical Analyses.
The total energy requirement of sows during lactation (TER, kcal ME/d) was calculated according to the formula of Noblet et al. (1990): TER = 110 x BW0.75 + (6.83 x LWG) - (125 x n), where BW (kg) = sow BW on d 1 postpartum, LWG (g/d) = litter weight gain over lactation, and n = the number of piglets per litter on d 5. The crude lysine requirement was estimated for a nil change in muscle weight over lactation (CMW, g/d), using the formula of Dourmad et al. (1998): CMW = -525 + 29.8 lysine - 0.392 LWG (R2 = 0.69). Energy and lysine balances were calculated by subtracting the calculated requirements from the actual intakes. The chemical composition of the BW on d 1, 7, 21, and 28 of lactation was estimated from the BW and P2 measurements using the equations proposed by Dourmad et al. (1997): lipid (kg) = -26.4 + 0.221 x EBW + 1.331 x P2 (R2 > 0.95); energy (Mcal) = -257 + 3.267 x EBW + 10.99 x P2 (R2 > 0.95); protein (kg) = 2.28 + 0.178 x EBW - 0.333 x P2 (R2 = 0.87); and water (kg) = 23.6 + 0.551 x EBW - 0.919 x P2 (R2 > 0.95), where EBW (kg) represents the sow empty live weight estimated from the live weight (EBW = 0.905 x BW1.013), and P2 is the backfat thickness at the last rib. The parity number (primiparous sows) and BW at farrowing of sows in the current study were similar to those from which the equations were developed.
Individual profiles of GH were analyzed for the determination of baseline and peak levels, according to the procedure described by Merriam and Wachter (1982).
Twenty-nine lactating primiparous sows were initially allocated to experimental treatments. Three sows (two sows from the C group and one sow from the L group) were withdrawn from the study because of low feed intake or aggressive behavior. Excluding these three females, data from 26 sows were used for statistical analyses of sow and litter performance (12 sows from the C group and 14 sows from L group), and data from 21 sows with catheters were used for analyses of hormones and metabolites (10 sows from C and 11 sows from L group). Only data from sows that were pregnant at slaughter were used for analyses of ovarian weight and ovulation rate (n = 19). The data were analyzed as a randomized complete block design, with two treatments in four replicates (blocks). Data were analyzed by ANOVA using the MIXED procedure of SAS (Littell et al., 1996, SAS Inst., Inc., Cary, NC). All models included the effects of the treatment (fixed effect) and of the replicate (random effect). All hormonal variables were controlled for normality using the Wilk-Shapiro test (SAS Inst., Inc.). All data for sow BW and backfat thickness changes, litter growth rate, insulin, GH, IGF-I, IGFBP, FSH, leptin, and metabolites were analyzed using repeated measures in MIXED procedures. The complete model included treatment, replicate, time, and time x treatment interaction as main effects. Sows were the experimental unit and significant differences among treatments were determined using sow within replicate x treatment interaction as the error term. Time effect was week effect for litter, day effect for sow performance, and preprandial and mean hormonal concentrations or sampling time effect for metabolite and hormone profiles. The effect of treatment on the number of pregnant sows was analyzed using Fisher’s Exact Test (SAS Inst., Inc.). Embryo survival data were arcsine-transformed before analysis. Pearson correlation analysis was used to determine the relationships between reproductive characteristics and hormone data on days W - 1 and W + 1 for sows with catheters (n = 21; SAS Inst., Inc.). In the results, the least squares means and the standard errors of least squares means are given.
|
Results
|
|---|
Litter and Sow Performance
There was neither a treatment effect nor a treatment x week interaction for LWG or ADG of the piglets, but there was a week effect (Table 2). Litters grew faster (P < 0.05) during wk 2 and 3 than during wk 1 and 4 of lactation.
View this table:
[in this window]
[in a new window]
|
Table 2. Litter performance during lactation from sows fed a low- (L, 10% CP and 0.5% lysine) or control (C, 20% CP and 1.08% lysine) protein diet (least squares means ± SEM)
|
|
As a result of the feed allowance imposed during lactation, there was no difference in daily feed consumption and energy intake among treatment groups (P > 0.10; Table 3). Estimated daily energy requirement for maintenance and milk production was similar in L and C sows. Therefore, all sows exhibited a negative energy balance during lactation (around -30%) that did not differ among treatment groups (P > 0.10; Table 3). In contrast, lysine intake was twofold higher (P < 0.001; Table 3) in C than in L sows. Because estimated daily lysine requirement was similar for all sows (mean: 46.6 g/d), lysine balance was very different between groups (P < 0.001). It was negative in L sows only.
View this table:
[in this window]
[in a new window]
|
Table 3. Feed intake, energy and lysine intakes, and calculated balances during lactation in low- (L, 10% CP and 0.5% lysine) or control (C, 20% CP and 1.08% lysine) protein diet sows (least squares means ± SEM)
|
|
There was a treatment x day interaction for BW during lactation (P < 0.001). Sow BW was similar among treatments at the start of lactation (Figure 1). From d 7, BW was lower in L than in C sows. The overall BW loss during lactation was higher in L than in C sows (L: 30 kg, C: 19 kg; P < 0.001). There were neither treatment effects nor day x treatment interactions for backfat thickness during lactation. However, overall backfat thickness decreased (P < 0.001) by 3.5 mm between d 7 and d 28 (Figure 1).
View larger version (14K):
[in this window]
[in a new window]
|
Figure 1. Changes in BW and backfat thickness during lactation in sows fed a low- (L = 10% CP and 0.5% lysine, n = 14) or control (C = 20% CP and 1.08% lysine, n = 12) protein diet during lactation. * and ** indicate difference in BW between groups, P < 0.05 and P < 0.01, respectively; a, b, c, and d indicate difference in backfat thickness between days, P < 0.01.
|
|
Estimated contents of sow’s body lipid, protein, and water did not differ among groups at farrowing (Table 4). Lipid, protein, and water contents decreased during lactation in all sows. There was a day x treatment interaction for protein and water contents (P < 0.001), but not for lipid content. After d 7, protein and water contents were lower in L than in C sows. Overall losses of lipids did not differ in C and L sows (mean: 10.3 kg), whereas protein and water losses were higher (P < 0.001) in L than in C sows (4.1 vs 2.0 kg and 13 vs 6 kg, respectively). At d 28, L and C sows had lost around 12% and 6% of their estimated protein content at farrowing, respectively.
View this table:
[in this window]
[in a new window]
|
Table 4. Estimated chemical composition and chemical composition change during lactation in sows fed a low- (L, 10% CP and 0.5% lysine) or control (C, 20% CP and 1.08% lysine) protein diet (least squares means ± SEM)
|
|
Metabolites
There was a significant treatment x sampling time interaction for most AA (Table 5). Preprandial plasma lysine concentration did not differ among treatment groups at the end of lactation. Preprandial plasma concentrations of histidine and methionine were higher (P < 0.05) in L than in C sows. In contrast, preprandial plasma concentrations of cystine and tryptophan were higher (P < 0.05) in C than in L sows. Preprandial concentrations of other AA in plasma were not affected by treatment (P > 0.10). After feeding, plasma concentrations of all AA increased significantly in C sows, whereas the increase was significant only for leucine, phenylalanine, tryptophan, histidine, proline, and tyrosine in L sows. There was no interaction for glutamine and alanine. Their concentrations were higher (P < 0.001) in L than in C sows (Table 5).
View this table:
[in this window]
[in a new window]
|
Table 5. Pre- and postprandial plasma amino acid concentrations 1 d before weaning in sows fed a low- (L, 10% CP and 0.5% lysine, n = 11) or control (C, 20% CP and 1.08% lysine, n = 10) protein diet during lactation (least squares means ± SEM)
|
|
Plasma profiles of glucose, urea, and NEFA concentrations of sows are shown in Figure 2. There was no treatment x sampling time interaction for plasma glucose on days W - 1 and W + 1, but there were treatment and sampling time effects. On day W - 1, mean plasma glucose concentration was higher (P < 0.02) in L than in C sows. It increased (P < 0.04) after the morning meal from 0915 to 1115, and slightly decreased at the end of sampling period in both treatments groups. On day W + 1, plasma glucose remained higher (P < 0.02) in L than in C sows, but glucose time-related variations were less marked than at the end of lactation. There was a treatment x sampling time interaction for plasma urea on day W - 1 (Figure 2). It increased (P < 0.04) after feeding in C sows, but did not change in L sows. It was higher (P < 0.001) in C than in L sows at all times. On day W + 1, there was neither a sampling time effect nor a treatment x sampling time interaction. Plasma urea remained higher (P < 0.02) in C than in L sows in spite of a decrease in urea concentration after weaning in C sows. There was neither a treatment effect nor a treatment x sampling time interaction for plasma NEFA concentrations on days W - 1 and W + 1, but there was a sampling time effect (Figure 2). Plasma NEFA concentrations decreased (P < 0.02) after the morning meal on days W - 1 and W + 1 in both treatment groups.
View larger version (36K):
[in this window]
[in a new window]
|
Figure 2. Plasma profiles of glucose, urea, and NEFA 1 d before or after weaning in sows fed a low- (L = 10% CP and 0.5% lysine, n = 11) or control (C = 20% CP and 1.08% lysine, n = 10) protein diet during lactation.  indicates time of feeding; T, S, and T x S indicate treatment effect, sampling time effect, or treatment x sampling time interaction, respectively. * P < 0.05.
|
|
Insulin, GH, IGF-I, IGFBP, FSH, and Leptin
Preprandial and mean plasma insulin, characteristics of GH profiles, mean FSH, and preprandial leptin concentrations are presented in Table 6. There was no treatment x day interaction for preprandial plasma insulin, but there were treatment and day effects. Preprandial plasma insulin was higher (P < 0.02) in C than in L sows and it was lower (P < 0.05) on day W - 1 than on day W + 1 in both treatment groups. For mean plasma insulin, there was a treatment x day interaction. Mean insulin concentrations were higher (P < 0.05) in C than in L sows on day W - 1, but not on day W + 1.
View this table:
[in this window]
[in a new window]
|
Table 6. Preprandial and mean plasma insulin, characteristics of growth hormone profiles, mean follicle-stimulating hormone, and preprandial leptin concentrations of sows 1 d before (W - 1) or 1 d after (W + 1) weaning (least squares means ± SEM)
|
|
Representative profiles of plasma GH on days W - 1 and W + 1 are illustrated in Figure 3. Concentrations of GH fluctuated at a high level at the end of lactation, whereas an episodic secretory pattern of GH was clear after weaning. There was a treatment x day interaction (P < 0.01) for mean and basal GH concentrations (Table 6
). Plasma mean and basal GH concentrations were higher (P < 0.05) in L than in C sows on day W - 1. They decreased (P < 0.05) after weaning in both treatment groups and there was no difference between L and C sows on day W + 1. There was neither a treatment effect nor a treatment x day interaction for GH pulse number. It decreased after weaning in both groups (P < 0.001).
View larger version (33K):
[in this window]
[in a new window]
|
Figure 3. Representative plasma GH profiles 1 d before (W - 1) or 1 d after (W + 1) weaning in sow # 920021 (group L) and sow # 930012 (group C). These sows received either a low- (L = 10% CP and 0.5% lysine) or control (C = 20% CP and 1.08% lysine) protein diet during lactation.
|
|
Daily plasma concentrations of IGF-I from day W - 1 to day W + 6 are presented in Figure 4. There was a treatment x day interaction for IGF-I concentration (P < 0.05). The IGF-I concentration was lower in L than in C sows on day W - 1 (P < 0.01) and on the day of weaning (P < 0.07). Plasma IGF-I concentrations increased (P < 0.01) after weaning in both treatment groups. There was no difference between groups (P > 0.10) from day W + 1 to day W + 6. Ligand blot analysis of IGFBP in plasma revealed the presence of five bands with apparent molecular masses of 43, 39, 34, 29, and 24 kDa, likely corresponding to IGFBP-3 (43 to 39 kDa) and BP-2 (34 kDa) and to unidentified IGFBP (29 kDa and 24 kDa). There was neither a treatment x day interaction nor a treatment effect for the relative IGFBP levels (Table 7). A trend (P < 0.07) for a decrease between day W - 1 and day W + 1 was observed for IGFBP-3, but not for the other IGFBP.
View larger version (16K):
[in this window]
[in a new window]
|
Figure 4. Plasma IGF-I concentrations measured once a day (1400) at the end of lactation (W - 1), day of weaning, and during the 6 d after weaning (W + 1 to W + 6) in sows fed a low- (L = 10% CP and 0.5% lysine, n = 11) or control (C = 20% CP and 1.08% lysine, n = 10) protein diet during lactation. Treatment effect: ** P< 0.01,  P < 0.07.
|
|
View this table:
[in this window]
[in a new window]
|
Table 7. Plasma insulin-like growth factor-binding protein levels of sows 1 d before (W - 1) or 1 d after (W + 1) weaning (least squares means ± SEM)
|
|
There was a treatment x day interaction for mean plasma FSH concentrations (P < 0.05; Table 6). Plasma FSH concentrations were similar in both experimental groups on day W - 1, but were higher (P < 0.05) in L than in C sows on day W + 1. There was a treatment x day interaction for preprandial plasma leptin concentration. Plasma leptin was similar among treatment groups on day W - 1, whereas it was higher (P < 0.01) in L than in C sows on day W + 1.
Reproductive Traits
All experimental sows returned to estrus within 9 d after weaning, and mean weaning-to-estrus interval did not differ between experimental groups (P > 0.10; Table 8). Nineteen out of 26 sows were pregnant at slaughter and the percentage rate of pregnant sows did not differ (P > 0.10) between L and C sows. The number of total (mean = 15.6 ± 1.3 embryos for all sows and 15.9 ± 1.3 for sows from endocrine data) and viable embryos and embryo survival rate did not differ between treatment groups (P > 0.10). However, L sows had a lower ovarian weight (P < 0.01) and ovulation rate (P < 0.05 for all sows and P < 0.07 for sows from the endocrine data set) than C sows.
Weaning-to-estrus interval was negatively correlated (P < 0.05) to mean plasma FSH and preprandial tryptophan concentrations at the end of lactation (Table 9). Ovulation rate was negatively correlated (P< 0.05) with preprandial concentrations of histidine and methionine. No associations between postweaning reproductive performance and plasma insulin, GH, IGF-I, leptin, and other preprandial metabolite concentrations were found (P > 0.10).
View this table:
[in this window]
[in a new window]
|
Table 9. Pearson correlation coefficients between the postweaning reproductive performance and concentrations of hormones and metabolites measured 1 d before weaning (W - 1)
|
|
|
Discussion
|
|---|
These results confirm that protein (lysine) restriction during lactation has marked effects on circulating metabolites and body reserve mobilization, and may have a detrimental influence on the reproductive function. To our knowledge, this is the first report looking at the consequences of protein restriction on the somatotropic hormones as well as on FSH and leptin. It clearly demonstrates marked effects for the somatotropic hormones during lactation and moderate effects for FSH and leptin just after weaning.
In the current study, the live weight of the experimental sows at farrowing is higher than that usually reported in the literature for primiparous sows, but within the range of weights of primiparous sows in commercial French herds (Caugant et al., 1999). However, these experimental sows are slightly leaner than young commercial sows around farrowing (16.2 mm backfat in the present experiment vs 18.1 mm in Caugant et al., 1999) and at the end of lactation (13.2 mm vs 14.4 mm backfat). This difference is probably due to genetic origin since experimental sows are crossbred with Piétrain, which is a lean genotype.
As expected, the actual lysine intake was close to the lysine required for maintenance and milk production in control sows (about 45 g/d; King et al., 1993; Dourmad et al., 1998; Yang et al., 2000b), whereas it was twofold less in L sows. The reduced concentration of plasma urea in L sows is likely the consequence of reduced protein intake, in agreement with Brendemuhl et al. (1987) and Yang et al. (2000c). As between-group differences in feed consumption were prevented by moderate feed restriction, energy intake averaged 70% of requirements for maintenance and milk production for all sows. This energy restriction provoked a loss of BW and backfat in all sows. Backfat loss during lactation and high concentrations of NEFA at the end of lactation were similar in the two experimental groups and reflected fat mobilization. In contrast, the live weight loss was higher in L than in C sows, essentially because of higher losses of body proteins and associated water. This is consistent with previous findings that demonstrated increased muscle protein degradation in sows fed inadequate amounts of lysine during lactation (Jones and Stahly, 1999a; Yang et al., 2000c). The increased mobilization of body proteins in L sows is illustrated by higher pre- and postprandial concentrations of plasma alanine and glutamine than that found in C sows, as described by Murray et al. (1999). Protein mobilization allows the L sows to prevent marked alterations in essential AA profiles, as shown by unaffected plasma concentrations of lysine, threonine, and branched-chain AA. However, it did not completely succeed, and preprandial concentrations of three essential AA were altered, being increased for methionine and histidine and decreased for tryptophan in L sows compared with C sows. Particularly, reduction in plasma tryptophan concentrations would be biologically important because this AA has a specific function as a precursor of brain serotonin, which participates in the central regulation of LH secretion (Vitale and Chiocchio, 1993; Lado-Abeal et al., 1997).
Decreasing protein (lysine) intake during lactation had no detrimental effect on LWG, in agreement with data from Revell et al. (1998). This indicates that mobilized protein reserves have been used to buffer protein-deficit impact and to maintain milk production throughout lactation. In contrast, Jones and Stahly (1999a) reported that low protein and/or AA intake during lactation reduced milk nutrient output, and hence, overall litter growth in primiparous sows. It should be noted that, in this previous study, litter size was standardized to 13 piglets and lysine restriction was more severe than in the current study (16 vs 21 g of lysine/d). Alternatively, these divergent findings may be explained by the different protein masses at farrowing: mean body protein content in our work was 34 vs 26 kg in the study of Jones and Stahly (1999a).
Reduction in the protein (lysine) content in the lactation diet resulted in a decrease in pre- and postprandial plasma insulin concentrations, in agreement with previous results (Tokach et al., 1992; Kusina et al., 1999; Yang et al., 2000c). The difference between groups in plasma insulin, in spite of a higher intake of carbohydrates in L vs C sows, is attributable to the amount of protein (AA) absorbed during the meal, since absorption of AA directly stimulates the pancreas to release insulin (Murray et al., 1999). Low insulin concentrations after feeding aid in decreasing the use of glucose and AA by muscle and adipose tissue and help promote the use of endogenous substrates (glycerol, AA) for gluconeogenesis (Chilliard et al., 1998; Grizard et al., 1999). This may explain the higher glucose concentrations found after feeding in L sows and increased protein mobilization.
The reduction of plasma IGF-I concentrations in response to protein (lysine) restriction is consistent with previous results in lactating sows. Plasma IGF-I decreased when lysine supply decreased from 56 to 36 g/d, but was not further modified when lysine intake decreased from 36 to 16 g/d or from 32 to 10 g/d (Kusina et al., 1999; Yang et al., 2000c). The levels of plasma IGFBP also were analyzed in the current study because they modulate IGF-I bioavailability. Their levels did not change in response to protein restriction. Under normal physiological conditions, IGF-I secretion by hepatic and nonhepatic tissues is stimulated by GH. In L sows, however, low IGF-I levels are associated with high plasma GH, indicating an uncoupling between IGF-I and GH. As suggested in feed- or protein-restricted animals by Thissen et al. (1994) and Breier (1999), this uncoupling could be due to a hepatic resistance to GH itself, which is related to low plasma insulin. In turn, the high concentrations of plasma GH in L sows would result from reduced concentrations of plasma IGF-I, and hence, attenuated negative feed-back action (Berelowitz et al., 1981; Le Roith et al., 2001). As GH and IGF-I are known to favor AA deposition in muscle tissue (Tomas et al., 1992; Breier, 1999), GH resistance could have facilitated mobilization of lean tissue in L sows.
Irrespective of treatment, weaning induced marked changes in sow endocrine and metabolic regulations. Plasma GH concentrations and pulse frequency were higher during late lactation than after weaning, due to the neuroendocrine stimuli elicited by piglets during suckling (Rushen et al., 1993). Patterns of secretion did not differ between L and C sows on day W + 1. Similarly, differences in plasma IGF-I concentrations were no longer significant by day W + 1, and they completely obliterated 3 d after weaning. This is consistent with previous findings that the IGF-I concentrations of feed-restricted sows are restored within a few days after weaning to levels comparable to those observed in well-fed sows (Carroll et al., 1996; Messias de Bragança and Prunier, 1999; van den Brand et al., 2001). The increase in peripheral IGF-I together with higher preprandial concentrations of glucose and insulin and lower NEFA concentrations after weaning in all sows indicate changes towards an anabolic state.
To our knowledge, no data are available on the influence of protein (lysine) restriction on plasma leptin concentrations. Recent evidence suggests that leptin is a metabolic signal to the reproductive system in the pig (Barb, 1999; Barb et al., 2001) and in other species (Barash et al., 1996; Tataranni et al., 1997). Leptin concentrations in the present study were similar to those previously described in sows during lactation (Mao et al., 1999; Estienne et al., 2000; Prunier et al., 2001). No difference in preprandial leptin concentrations occurred among treatment groups on day W - 1, in agreement with Mao et al. (1999), who demonstrated that total feed restriction did not alter preprandial plasma leptin at the end of lactation. However, an increase in preprandial leptin concentration was observed between days W - 1 and W + 1 in protein-restricted sows, but not in control sows. Changes in leptin occurred in the absence of change in backfat thickness, and there was no association between leptin and insulin on days W - 1 or W + 1 (data not shown). These changes are likely related to the metabolic and/or endocrine changes that occurred in L sows around weaning. Further research is needed to elucidate the underlying physiological mechanism.
Contrasting with previous findings (King and Williams, 1984b; Brendemuhl et al., 1987; Jones and Stahly, 1999b), the return to estrus after weaning was not delayed by protein (lysine) restriction throughout lactation. The large body reserves of our sows at farrowing and weaning (210 kg of live weight at farrowing vs 150 to170 kg in the previous experiments of King and Williams [1984b] and Jones and Stahly [1999b]), could have buffered the negative effect of protein restriction on the weaning-to-estrus interval. This hypothesis is supported by the concept that nutrient intakes, body reserve losses, and absolute amount of maternal reserves at farrowing interact to influence reproductive performance (Mullan and Williams, 1989; Yang et al., 1989; Dourmad, 1991). This is also in agreement with the results of King (1987) and Charette et al. (1995), who observed that the weaning-to-estrus interval after first lactation was closely related to body protein or BW at weaning, with heavy primiparous sows having weaning-to-estrus intervals similar to that of multiparous sows.
Protein restriction during lactation reduced ovulation rates at postweaning estrus. Most studies reported no impact of feed restriction (King and Williams, 1984a; Kirkwood et al., 1987, 1990) or protein restriction (King and Williams,1984b; King and Dunkin, 1986) during lactation on postweaning ovulation rate and subsequent litter size, while postweaning estrus was clearly delayed. In two experiments, a lower ovulation rate was reported in response to feed restriction during all or part of lactation (15 vs 20, P < 0.05, Zak et al., 1997a; 16 vs 18, P = 0.08, van den Brand et al., 2000). In these two experiments, all sows exhibited estrus within 5 to 8 d after weaning. Moreover, it was previously reported that feed-restriction during lactation alters the number or distribution of medium-sized follicles (1 to 4 mm) at weaning (Quesnel et al., 1998). Therefore, when the weaning-to-estrus interval is short, it is likely that sows have no time to recover from detrimental effects of catabolic state on follicular growth during lactation, as previously suggested (Clowes et al., 1994; Zak et al., 1997b).
Mechanisms mediating the metabolic effects on ovulation rate are not clear. In contrast to the induction of ovulation, which mainly depends on pulsatile secretion of LH, ovulation rates are greatly influenced by insulin and growth factors acting in synergy with FSH (reviewed by Hunter et al., 1992; Monget and Martin, 1997). Therefore, it is plausible that the reduced concentrations of insulin and IGF-I in lactating L sows are involved in the reduced ovulation rate, although the lack of relationships between insulin or IGF-I and ovulation rate in the present study does not support this hypothesis. In turn, the higher concentrations of FSH in L sows just after weaning could be the consequence of the less active folliculogenesis and attenuated negative feedback action from the ovaries. Mullan et al. (1991) reported a similar effect of feed restriction on FSH concentrations at the end of lactation and after weaning. Finally, high concentrations of GH may also have played a role in reduced ovulation rate, since overexpression of GH gene by transgenic prepuberal gilts reduces the number of large follicles and alters steroidogenesis (Guthrie et al., 1993). However, a stimulatory influence of exogenous GH on folliculogenesis also was reported in cyclic gilts (Kirkwood et al., 1988) and primiparous weaned sows (Whitley et al., 1998). Thus, the involvement of elevated plasma GH in ovulation rate remains questionable.
Despite the reduction in ovulation rate, protein (lysine) restriction had no significant influence on the number of viable embryos in early gestation, suggesting little or no influence on the subsequent litter size. This is in agreement with previous experiments that reported no effect on litter size at birth when lysine intakes during the first lactation varied between 28 and 45 g/d (Tritton et al., 1996; Touchette et al., 1998; Yang et al., 2000b). Nevertheless, it cannot be ruled out that such a reduction in ovulation rate results in reduced litter size at birth in commercial herds, where breeding conditions are detrimental for embryo survival (e.g., low herd health, low feed consumption during lactation).
In conclusion, these results provide evidence that protein (lysine) restriction during lactation moderately alters profiles of plasma essential AA and markedly changes plasma concentrations of GH, IGF-I, and insulin. The restriction had no effect on the weaning-to-estrus interval, likely due to the protective effect of a relatively high-protein mass at farrowing, but it had a negative influence on the ovulation rate. Data did not show associations between metabolic hormones and ovulation rate.
|
Implications
|
|---|
High body protein reserves at farrowing may buffer the negative impact of dietary protein (lysine) restriction on milk production, and may also minimize alterations in reproductive performance when protein intake during lactation is low. High growth hormone concentrations, together with low insulin-like growth factor-I and insulin levels are good markers of a lactating sow’s metabolic adaptation to nutritional treatment.
|
Footnotes
|
|---|
1 The authors wish to acknowledge M. Massard, Y. Lebreton, and Y. Collaux for their expert technical assistance. The authors also thank Y. Combarnous (INRA/CNRS/Univ. Tours, Nouzilly, France) for the gift of highly purified porcine FSH for iodination; I. Louveau (INRA Saint-Gilles, France), and U. Weiler (University of Hohenheim, Germany) for providing antiserum against IGF-I and NHPP, NIDDK; and A. F. Parlow (Torrance, Ca) for providing pGH-Bio. 
2 C. Mejia-Guadarrama was supported by a scholarship from CONACYT/INIFAP (Mexico) and SFERE (France).
Received for publication April 17, 2002.
Accepted for publication July 24, 2002.
|
Literature Cited
|
|---|
Barash, I. A., C. C. Cheung, D. S. Weigle, H. Ren, E. B. Kabigting, J. L. Kuijper, K. Donald, C. Steiner, and R. Steiner. 1996. Leptin is a metabolic signal to the reproductive system. Endocrinology 137:3144–3147.[Abstract]
Barb, C. R. 1999. The brain-pituitary-adipocyte axis: Role of leptin in modulating neuroendocrine function. J. Anim. Sci. 77:1249–1257.[Abstract/Free Full Text]
Barb, C. R., J. B. Barrett, R. Kraeling, and G. B. Rampacek. 2001. Serum leptin concentrations, luteinizing hormone and growth hormone secretion during feed and metabolic fuel restriction in the prepuberal gilt. Domest. Anim. Endocrinol. 20:47–63.[Medline]
Berelowitz, M., M. Szabo, L. A. Frohman, S. Firestone, L. Chu, and R. L. Hintz. 1981. Somatomedin-C mediates growth hormone negative feed-back by effects on both the hypothalamus and the pituitary. Science (Washington, DC) 212:1279–1281.[Abstract/Free Full Text]
Breier, B. H. 1999. Regulation of protein and energy metabolism by the somatotropic axis. Domest. Anim. Endocrinol. 17:209–218.[Medline]
Brendemuhl, J. H., A. Lewis, and E. R. Peo, Jr. 1987. Effect of protein and energy intake by primiparous sows during lactation on sow and litter performance and sow serum thyroxine and urea concentrations. J. Anim. Sci. 64:1060–1069.[Abstract/Free Full Text]
Carroll, C. M., P. Lynch, M. P. Boland, L. J. Spicer, F. H. Austin, N. Leonard, W. J. Enright, and J. F. Roche. 1996. The effects of feed intake during lactation and post weaning on the reproductive performance and hormone and metabolite concentrations of primiparous sows. Anim. Sci. 63:297–306.
Camous, S., A. Prunier, and J. Pelletier. 1985. Plasma prolactin, LH, FSH and estrogen excretion patterns in gilts during sexual development. J. Anim. Sci. 60:1308–1317.[Abstract/Free Full Text]
Caugant, A., H. Roy, and J. Y. Dourmad. 1999. Evolution des réserves corporelles chez la jeune truie et performances à la première mise-bas. J. Rech. Porcine Fr. 31:1–7.
Charrette, R., M. Bigras-Poulin, and G. P. Martineau. 1995. Une méta-analyse de l’anoestrus nutritionnel chez la truie. J. Rech. Porcine Fr. 27:31–36.
Chilliard, Y., F. Bocquier, and M. Doreau. 1998. Digestive and metabolic adaptations of ruminants to undernutrition, and consequences on reproduction. Reprod. Nutr. Dev. 38:131–152.[Medline]
Clowes, E. J., F. X. Aherne, and G. R. Foxcroft. 1994. Effect of delayed breeding on the endocrinology and fecundity of sows. J. Anim. Sci. 72:283–291.[Abstract]
Dourmad, J.Y. 1991. Effect of feeding level in the gilt during pregnancy on voluntary feed intake during lactation and changes in body composition during gestation and lactation. Livest. Prod. Sci. 27:309–319.
Dourmad, J. Y., M. Etienne, J. Noblet, and D. Causeur. 1997. Prédiction de la composition chimique des truies reproductrices à partir du poids vif et de l’épaisseur de lard dorsal. J. Rech. Porcine Fr. 29:255–262.
Dourmad, J. Y., J. Noblet, and M. Etienne. 1998. Effect of protein and lysine supply on performance, nitrogen balance, and body composition changes of sows during lactation. J. Anim. Sci. 76:542–550.[Abstract/Free Full Text]
Estienne, M. J., A. F. Harper, C. R. Barb, and M. J. Azain. 2000. Concentrations of leptin in serum and milk collected from lactating sows differing in body condition. Domest. Anim. Endocrinol. 19:275–280.[Medline]
Grizard, J., D. Dardevet, M. Balage, D. Larbaud, S. Sinaud, I. Savary, K. Grzelkowska, C. Rochon, I. Tauveron, and C. Obled. 1999. Insulin action on skeletal muscle protein metabolism during catabolic states. Reprod. Nutr. Dev. 39:61–74.[Medline]
Guthrie, H. D., V. G. Pursel, D. J. Bolt, and B. S. Cooper. 1993. Expression of a bovine growth hormone transgene inhibits pregnant mare’s serum gonadotropin-induced follicle maturation in prepuberal gilts. J. Anim. Sci. 71:3409–3413.[Abstract]
Hossenlopp, P., D. Seurin, B. Segovia-Quinson, and M. Binoux. 1986. Identification of an insulin-like growth factor binding protein in human cerebrospinal fluid with a selective affinity for IGF-II. FEBS Lett. 208:439–444.[Medline]
Hunter , M. G., C. Biggs, L. S. Faillace, and H. M. Picton. 1992. Current concepts of folliculogenesis in monoovular and polyovular farm species. J. Reprod. Fertil. 45(Suppl.):21–38.
INRA. 1989. L’alimentation des animaux monogastriques. 2nd ed. Institut National de la Recherche Agronomique, Paris, France.
Jones, D. B., and T. S. Stahly. 1999a. Impact of amino acid nutrition during lactation on body nutrient mobilization and milk nutrient output in primiparous sows. J. Anim. Sci. 77:1513–1522.[Abstract/Free Full Text]
Jones, D. B., and T. S. Stahly. 1999b. Impact of amino acid nutrition during lactation on luteinizing hormone secretion and return to estrus in primiparous sows. J. Anim. Sci. 77:1523–1531.[Abstract/Free Full Text]
King, R. H. 1987. Nutritional anoestrus in young sows. Pig News Info. 1:15–22.
King, R. H., and A. C. Dunkin. 1986. The effect of nutrition on the reproductive performance of first-litter sows. 4. The relative effects of energy and protein intakes during lactation on the reproductive performance of sows and their piglets. Anim. Prod. 43:319–325.
King, R. H., M. S. Toner, H. Dove, C. S. Atwood, and W. G. Brown. 1993. The response of first-litter sows to dietary protein level during lactation. J. Anim. Sci. 71:2457–2463.[Abstract]
King, R. H., and I. H. Williams. 1984a. The effect of nutrition on the reproductive performance of first-litter sows. 1. Feeding level during lactation and between weaning and mating. Anim. Prod. 38:241–247.
King, R. H., and I. H. Williams. 1984b. The effect of nutrition on the reproductive performance of first-litter sows. 2. Protein and energy intakes during lactation. Anim. Prod. 38:249–256.
Kirkwood, R. N., S. K. Baidoo, and F. X. Aherne. 1990. The influence of feeding level during lactation and gestation on the endocrine status and reproductive performance of second parity sows. Can. J. Anim. Sci. 70:1119–1126.
Kirkwood, R. N., S. K. Baidoo, F. X. Aherne, and A. P. Sather. 1987. The influence of feeding level during lactation on the occurrence and endocrinology of the postweaning estrus in sows. Can. J. Anim. Sci. 67:405–415.
Kirkwood, R. N., P. A. Thacker, A. D. Gooneratne, B. L. Guedo, and B. Laarveld. 1988. The influence of exogenous growth hormone on ovulation rate in gilts. Can. J. Anim. Sci. 68:1097–1103.
Kusina, J., J. E. Pettigrew, A. F. Sower, M. E. White, B. A. Crooker, and M. R. Hathaway. 1999. Effect of protein intake during gestation and lactation on the lactational performance of primiparous sows. J. Anim. Sci. 77:931–941.[Abstract/Free Full Text]
Lado-Abeal, J., C. Rey, J. M. Cabezas-Agricola, A. Rodriguez, E. Camarero, and J. Cabezas-Cerrato. 1997. L-hydroxytryptophan amplifies pulsatile secretion of LH in the follicular phase of normal women. Clin. Endocrinol. 47:555–563.[Medline]
Le Roith, D., C. Bondy, S. Yakar, J. Liu, and A. Butler. 2001. The somatomedin hypothesis: 2001. Endocrine Rev. 22:53–74.[Abstract/Free Full Text]
Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS System for Mixed Models. SAS Institute Inc., Cary, NC.
Louveau, I., and M. Bonneau. 1996. Effect of a growth hormone infusion on plasma insulin-like growth factor-I in Meishan and Large White pigs. Reprod. Nutr. Dev. 36:301–310.[Medline]
Louveau, I., M. Bonneau, and D. N. Salter. 1991. Age-related changes in plasma porcine growth hormone (GH) profiles and insulin-like growth factor-I (IGF-I) concentrations in Large White and Meishan pigs. Reprod. Nutr. Dev. 31:205–216.[Medline]
Mao, J., L. J. Zak, J. R. Cosgrove, S. Shostak, and G. R. Foxcroft. 1999. Reproductive, metabolic, and endocrine responses to feed restriction and GnRH treatment in primiparous, lactating sows. J. Anim. Sci. 77:724–735.[Abstract/Free Full Text]
Merriam, G. R., and K. W. Wachter. 1982. Algorithms for the study of episodic hormone secretion. Am. J. Physiol. 243:E310–E318.[Medline]
Messias de Bragança, M., and A. Prunier. 1999. Effects of low feed intake and hot environment on plasma profiles of glucose, nonesterified fatty acids, insulin, glucagon, and IGF-I in lactating sows. Domest. Anim. Endocrinol. 16:89–101.[Medline]
Monget , P., and G. B. Martin. 1997. Involvement of insulin-like growth factors in the interactions between nutrition and reproduction in female mammals. Hum. Reprod. 12:33–52.[Medline]
Mullan, B. P., W. H. Close, and G. R. Foxcroft. 1991. Metabolic state of the lactating sows influences plasma LH and FSH before and after weaning. Page 31 in Manipulating Pig Production. E. S. Battersham, ed. Australasian Pig Sci. Assoc., Werribee, Australia.
Mullan, B. P., and I. H. Williams. 1989. The effect of body reserves at farrowing on the reproductive performance of first litter sows. 1. Feeding level during lactation, and between weaning and mating. Anim. Prod. 38:241–247.
Murray, R. K., D. K. Granner, P. A. Mayes, and V. W. Rodwell. 1999. Harper Biochimie. 24th ed. McGraw-Hill International Ltd., Berkshire, UK.
Noblet, J., J. Y. Dourmad, and M. Etienne. 1990. Energy utilization in pregnant and lactating sows: Modeling of energy requirements. J. Anim. Sci. 68:562–572.[Abstract]
NRC. 1988. Pages 49–53 in Nutrient Requirements of Swine. 9th ed. Natl. Acad. Press, Washington, DC.
O’Grady, J. F., P. B. Lynch, and P. A. Kearney. 1985. Voluntary feed intake by lactating sows. Livest. Prod. Sci. 12:355–365.
Prunier, A., C. Martin, A. M. Mounier, and M. Bonneau. 1993. Metabolic and endocrine changes associated with undernutrition in the peripubertal gilt. J. Anim. Sci. 71:1887–1894.[Abstract]
Prunier, A., C. A. Mejia Guadarrama, J. Mourot, and H. Quesnel. 2001. Influence of feed intake during pregnancy and lactation on fat body reserve mobilisation, plasma leptin and reproductive function of primiparous lactating sows. Reprod. Nutr. Dev. 41:333–347.[Medline]
Prunier, A., and H. Quesnel. 2000. Nutritional influences on the hormonal control of reproduction in female pigs. Livest. Prod. Sci. 63:1–19.
Qian, H., C. R. Barb, M. M. Compton, G. J. Hausman, M. J. Azain, R. R. Kraeling, and C. A. Baile. 1999. Leptin mRNA expression and serum leptin concentrations as influenced by age, weight and estradiol in pigs. Domest. Anim. Endocrinol. 16:135–143.[Medline]
Quesnel, H., A. Pasquier, A. M. Mounier, and A. Prunier. 1998. Influence of feed restriction during lactation on gonadotropic hormones and ovarian development in primiparous sows. J. Anim. Sci. 76:856–863.[Abstract/Free Full Text]
Revell, D. K., I. H. Williams, B. P. Mullan, J. L. Ranford, and R. J. Smits. 1998. Body composition at farrowing and nutrition during lactation affect the performance of primiparous sows: II. Milk composition, milk yield, and pig growth. J. Anim. Sci. 76:1738–1743.[Abstract/Free Full Text]
Rushen, J., G. R. Foxcroft, and A. M. De Passillé. 1993. Nursing-induced changes in pain sensitivity, prolactin, and somatotropin in the pig. Physiol. Behav. 53:265–270.[Medline]
Schams, D., B. Berisha, M. Kosmann, R. Einspanier, and W. M. Amselgruber. 1999. Possible role of growth hormone, IGFs, and IGF-I binding proteins in the regulation of ovarian function in large farm animals. Domest. Anim. Endocrinol. 17: 279–285.[Medline]
Schams, D., W. D. Kratzl, G. Brem, and F. Graf. 1994. Secretory pattern of metabolic hormones in the lactating sow. Exp. Clin. Endocrinol. 102:439–447.[Medline]
Sève, B., M. C. Meunier-Salaün, M. Monnier, Y. Colléaux, and Y. Henry. 1991. Impact of dietary tryptophan and behavioral type on growth performance and plasma amino acids of young pigs. J. Anim. Sci. 69:3679–3688.[Abstract]
Tataranni, P. A., M. B. Monroe, C. A. Dueck, S. A. Traub, M. Nicolson, M. M. Manore, K. S. Matt, and E. Ravussin. 1997. Adiposity, plasma leptin concentration and reproductive function in active and sedentary females. Int. J. Obes. Relat. Metab. Disord. 21:818–821.[Medline]
Thissen, J. P., J. M. Ketelslegers, and L. E. Underwood. 1994. Nutritional regulation of the insulin-like growth factors. Endocrine Rev. 15:80–101.[Abstract]
Tokach, M. D., J. E. Pettigrew, G. D. Dial, J. E. Wheaton, B. A. Crooker, and L. J. Johnston. 1992. Characterization of luteinizing hormone secretion in the primiparous, lactating sow: Relationship to blood metabolites and return-to-estrus interval. J. Anim. Sci. 70:2195–2201.[Abstract]
Tomas, F. M., R. G. Campbell, R. H. King, R. J. Johnson, C. S. Chandler, and M. R. Taverner. 1992. Growth hormone increases whole-body protein turnover in growing pigs. J. Anim. Sci. 70:3138–3143.[Abstract]
Touchette, K. J., G. L. Allee, M. D. Newcomb, and R. D. Boyd. 1998. The lysine requirement of lactating primiparous sows. J. Anim. Sci. 76:1091–1097.[Abstract/Free Full Text]
Tritton, S. M., R. H. King, R. G. Campbell, A. C. Edwards, and P. E. Hughes. 1996. The effects of dietary protein and energy levels of diets offered during lactation on the lactational and subsequent reproductive performance of first-litter sows. Anim. Sci. 62:573–579.
van den Brand, H., S. J. Dieleman, N. M. Soede, and B. Kemp. 2000. Dietary energy source at two feeding levels during lactation in primiparous sows: I. Effects on glucose, insulin and luteinizing hormone and on follicle development, weaning-to-estrus interval, and ovulation rate. J. Anim. Sci. 78:396–404.[Abstract/Free Full Text]
van Den Brand, H., A. Prunier, N. M. Soede, and B. Kemp. 2001. In primiparous sows, plasma insulin-like growth factor-I can be affected by lactational feed intake and dietary energy source and is associated with luteinizing hormone. Reprod. Nutr. Dev. 41:27–39.[Medline]
Vitale, M. L., and S. R. Chiocchio. Serotonin, a neurotransmitter involved in the regulation of luteinizing hormone release. Endocrine Rev. 14:480–493.
Whitley, N. C., A. B. Moore, and N. M. Cox. 1998. Comparative effects of insulin and porcine somatotropin on postweaning follicular development in primiparous sows. J. Anim. Sci. 76:1455–1462.[Abstract/Free Full Text]
Yang, H., P. R. Eastham, P. Phillips, and C. T. Whittemore. 1989. Reproductive performance, BW and body composition of breeding sows with differing body fatness at parturition, differing nutrition during lactation, and differing litter size. Anim. Prod. 48:181–201.
Yang, H., G. R. Foxcroft, J. E. Pettigrew, L. J. Johnston, G. C. Shurson, A. N. Costa, and L. J. Zak. 2000a. Impact of dietary lysine during lactation on follicular development and oocyte maturation after weaning in primiparious sows. J. Anim. Sci. 78:993–1000.[Abstract/Free Full Text]
Yang, H., J. E. Pettigrew, L. J. Johnston, G. C. Shurson, and R. D. Walker. 2000b. Lactational and subsequent reproductive responses of lactating sows to dietary lysine (protein) concentration. J. Anim. Sci. 78:348–357.[Abstract/Free Full Text]
Yang, H., J. E. Pettigrew, L. J. Johnston, G. C. Shurson, J. E. Wheaton, M. E. White, Y. Koketsu, A. F. Sower, and J. A. Rathmacher. 2000c. Effects of dietary lysine intake during lactation on blood metabolites, hormones, and reproductive performance in primiparous sows. J. Anim. Sci. 78:1001–1009.[Abstract/Free Full Text]
Zak, L. J., J. R. Cosgrove, F. X. Aherne, and G. R. Foxcroft. 1997a. Pattern of feed intake and associated metabolic and endocrine changes differentially affect postweaning fertility in primiparous lactating sows. J. Anim. Sci. 75:208–216.[Abstract/Free Full Text]
Zak, L. J., X. Xu, R. T. Hardin, and G. R. Foxcroft. 1997b. Impact of different patterns of feed intake during lactation in the primiparous sow on follicular development and oocyte maturation. J. Reprod. Fertil. 110:99–106.[Abstract]
This article has been cited by other articles:
|
|
|
|
 
J. E. Chavarro, J. W. Rich-Edwards, B. A. Rosner, and W. C. Willett
Diet and Lifestyle in the Prevention of Ovulatory Disorder Infertility
Obstet. Gynecol.,
November 1, 2007;
110(5):
1050 - 1058.
[Abstract]
[Full Text]
[PDF]
|
|
|
Top
Abstract
Introduction
