J. Anim Sci. 2007. 85:118-128. doi:10.2527/jas.2006-158
© 2007 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Influence of litter size on metabolic status and reproductive axis in primiparous sows1
H. Quesnel2,
M. Etienne and
M.-C. Père
INRA, UMR Livestock Production Systems, Animal and Human Nutrition, 35590 Saint-Gilles, France
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Abstract
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This study on primiparous sows was designed to 1) determine the impact of nursing a large litter on LH secretion and follicular development, and 2) investigate the metabolic adaptations by which milk yield increases with litter size. At farrowing, crossbred, primiparous sows were assigned to 1 of 3 experimental groups differing in litter size and feed allowance. Sows with 13 or 14 piglets (13AL, n = 7) were fed ad libitum. Sows with 7 piglets were fed ad libitum (7AL, n = 6) or were feed-restricted (7R, n = 8). The restriction was based on the estimated energy deficiency for the 13AL sows. On d 9 ± 1 of lactation, a jugular catheter was surgically implanted. Serial blood samplings and glucose tolerance tests were performed in mid- and late lactation. Sows were slaughtered 3 d after weaning, and ovarian characteristics were recorded. During lactation, the 7AL sows lost no or little body reserves, and their estimated energy balance was near zero. The 13AL and 7R sows exhibited similar negative energy balances and similar losses of backfat and estimated lipid content. Litter growth rate was greater (P < 0.05) in the 13AL than in the 7AL and 7R groups. After weaning, the volume of the largest 14 follicles was smaller (P < 0.05) in sows nursing 13 or 14 piglets than in sows with 7 piglets. Plasma concentrations of LH and LH pulse frequency did not differ between groups (P > 0.1). The longer glucose half-life on d 16 than on d 27 of lactation (22.5 vs. 18.8 min; P < 0.05) indicated a lower glucose tolerance in mid- than in late lactation. The area under the insulin curve was greater in the 7AL than in the 13AL sows (P = 0.08) and intermediate in the 7R group, with no differences in glucose profiles. This led to the suggestion that the 7AL sows were more resistant to insulin than the 13AL sows. In all groups of sows, follicular development after weaning was correlated with LH secretion in midlactation. Active follicular development was associated with prolonged secretion of insulin in response to glucose challenge. Our results show that besides litter size, a sow’s metabolic status in lactation influences follicular maturation after weaning and also indicate that the metabolic adaptations by which primiparous sows nursing large litters increase litter growth rate and body reserve mobilization do not involve an accentuated peripheral insulin resistance.
Key Words: insulin • lactation • litter size • metabolism • reproduction • sow
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INTRODUCTION
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Litter size of sows has greatly increased during the past decade. The number of nursed piglets is a determining factor of milk production (Etienne et al., 2000
) and thus of the sow’s energy and nutrient requirements. Voluntary feed intake usually increases with litter size but often remains insufficient to satisfy nutrient needs during the first lactation (Dourmad, 1988). As a consequence, primiparous sows nursing large litters lose generally more BW throughout lactation than sows nursing smaller litters (Auldist et al., 1998; Kim and Easter, 2001).
To our knowledge, however, data on the physiological mechanisms that allow sows to maintain high milk production are scarce. Besides, increasing litter size is likely to intensify the stimuli originating from the piglets, which were demonstrated to inhibit the activity of the hypothalamic-pituitary axis (Cox and Britt, 1982). The increased nutritional deficiency and udder stimulation together could amplify the inhibition of GnRH and LH secretion in late lactation (Foxcroft, 1992; Quesnel and Prunier, 1995). This could delay return to estrus after weaning, especially in primiparous females prone to reproductive problems or bred in suboptimal herd conditions. Such a consequence was demonstrated in feed-restricted primiparous sows. A small delay in the onset of estrus after weaning has been associated with a reduction in subsequent reproductive performance (litter size and farrowing rate; Leman, 1990; Vesseur et al., 1994).
The aims of the present experiment were to 1) determine the influence of nursing a large litter on LH secretion and follicular development, and 2) investigate the metabolic adaptations by which milk yield increases when litter size increases.
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MATERIALS AND METHODS
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Animals and Experimental Design
The animals used in the experiment were reared in compliance with national regulations for the humane care and use of animals in research. The experiment was conducted in 5 replicates on a total of 28 Pietrain x (Landrace x Large White) crossbred gilts, which were inseminated with semen from Pietrain boars. They were housed individually during the first month of gestation and in groups thereafter and had a BW of 171 ± 7 kg at 4 wk after insemination.
The gilts were moved from the gestation to the farrowing rooms at 104 ± 1 d of gestation and were kept in individual farrowing crates (2 x 2.5 m). Room temperature was maintained between 20 and 25°C, and artificial light was provided by incandescent lamps for 10 h/ d. Parturition was induced by a single intramuscular 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 (d 0 of lactation).
To dissociate the respective influence of suckling stimuli and nutritional deficiency on reproduction, sows were assigned to 1 of 3 experimental groups after farrowing: sows nursing 13 or 14 piglets and fed ad libitum (13AL), and sows with 7 piglets and fed ad libitum (7AL) or feed-restricted (7R). Crossfostering occurred within 48 h after birth to standardize the litters to 13 or 14 or to 7 piglets. Throughout lactation, no creep feed was given to the piglets. The piglets were weaned between 0830 and 0930 at 30 ± 1 d of age. Water was freely available for the sows and the piglets throughout the experimental period.
During gestation, the sows were fed 2.5 kg/d of a conventional gestation diet containing 12.5 MJ of ME/ kg, 13.5% CP, and 0.5% Lys (on an as-fed basis; Table 1). The daily feed allowance was provided in 2 equal meals around 0830 and 1430. During lactation, they received a standard lactation diet providing 13.0 MJ of ME/kg, 17.3% CP, and 0.8% Lys (as-fed basis; Table 1). On d 0, 1, and 2 postpartum, the sows were allowed to consume 1, 2.5, and 3.5 kg/d of the lactation diet, respectively. Thereafter, the amount of feed depended on the group. Sows with 13 or 14 piglets (13AL) were fed a high level of feeding, but not ad libitum, to prevent large differences in feed consumption. Sows with 7 piglets were fed ad libitum (7AL) or restricted (7R). The restriction was based on the estimated energy deficiency for the 13AL sows based on data previously obtained in our experimental herd (described in Calculations and Statistical Analyses). Feed refusals were weighed daily before the morning meal, and the actual feed intake was then calculated. From the day of weaning until slaughter 3 d later, all sows remained in their farrowing crate and were fed 2.5 kg/d of the gestation diet.
Sows were slaughtered at a local abattoir, and reproductive tracts were collected immediately after death. Both ovaries were weighed, and follicles larger than 4 mm in diam. were counted. The surface diam. of the largest 14 follicles was determined using a caliper. Follicular fluid was collected by aspiration from these same follicles and weighed.
Glucose Tolerance Tests and Blood Sampling
On d 9 ± 1 of lactation, an indwelling Silastic catheter (Dow Corning, Midland, MI; 2.16 mm o.d., 1.02 mm i.d.) was implanted under general anesthesia through a collateral vein into the right jugular vein of all sows, as previously described (Père et al., 2000). Sows were deprived of feed for 14 h before surgery. Approximately 1 h after surgery, sows returned to their farrowing crate and were immediately refed. During lactation, catheters were flushed 3 times weekly with 10 mL of saline solution (154 mM NaCl) containing 250 IU of heparin/ mL (Sanofi-Synthelabo, Le Plessis-Robinson, France).
In midlactation (d 15 ± 1) and on the day before weaning (d 29 ± 1), serial blood samples (2 mL) were collected every 15 min from 0815 to 1615. Additionally, a single blood sample (3 mL) was taken at 0830 three days after weaning.
Glucose tolerance tests were performed as previously described (Père et al., 2000), on d 16 ± 1 and d 27 ± 1 of lactation, after an overnight feed withdrawal. A sterile glucose solution (1.665 M) was injected into the jugular catheter to deliver 0.5 g of glucose/kg of BW. Twenty milliliters of saline solution was then injected to rinse the catheter. The first blood sample was drawn immediately afterwards, at a time considered as time zero. Blood samples (2 to 3 mL) were drawn at 15 and 2 min before the test and at 3, 6, 10, 15, 20, 25, 30, 35, 40, 50, 60, and 70 min. Blood samples were collected with heparinized syringes, placed on ice, and immediately centrifuged for 2 min at 8,500 x g at 4°C. The supernatants were divided into 2 subsamples and stored at – 20°C until they were analyzed.
Measurements
P iglets were weighed at birth and at 7, 14, 21, and 29 ± 1 d of age. Sows were weighed at d 1, 9, and 26 of lactation and at weaning. Each sow’s backfat thickness was ultrasonically measured (Sonolayer SAL-32B, Toshiba, Tokyo, Japan), after farrowing and at weaning, on each side at 65 mm from the dorsal midline at the level of the last rib (P2).
Analyses
Hormone Assays.
Plasma concentrations of hormones were determined in duplicate in validated double-antibody RIA, within a single assay. For the LH assay (Camous et al., 1985), the intraassay CV was 11% at 0.73 ng/mL, and the average sensitivity was 0.3 ng/ mL (95% of total binding). Plasma concentrations of IGF-I were determined after an acid-ethanol extraction. The assay and the extraction technique were validated for plasma samples from lactating and weaned sows (Louveau and Bonneau, 1996). The intraassay CV was 7.4% at 258 ng/mL, and the average sensitivity was 7.5 ng/mL. For insulin assays (Prunier et al., 1993), the intraassay CV was 6% at 89.0 µIU/mL, and the average sensitivity was 3 µIU/mL.
Concentrations of LH were determined every 15 min for 8 h on d 15 and 29, and those of IGF-I were determined once at 0830 on d 15 and 29 of lactation and 3 d after weaning. Concentrations of insulin were measured in all samples from the glucose tolerance tests.
Metabolite Assays.
Plasma concentrations of glucose and NEFA were measured by enzymatic methods (bioMérieux kits ref 61272, Marcy l’Etoile, France; Wako Chemical NEFA C, Neuss, Germany) adapted to a Cobas Mira multichannel analyser (Roche, Basel, Switzerland). The average sensitivity was 19 and 3 µM for glucose and NEFA, respectively. Concentrations of glucose were measured in each sample from the glucose tolerance test; NEFA were measured only on the 2 samples obtained before the injection of glucose.
Calculations and Statistical Analyses
Total energy requirement (TER, kJ of ME/d) of sows during lactation was calculated according to the formula of Noblet et al. (1990): TER = (460 x BW0.75) + (28.5 x LWG) – (523 x n), where BW (kg) = average sow BW during lactation, LWG (g/d) = litter weight gain over lactation, and n = the number of piglets per litter on d 3. Energy balance was calculated by subtracting the calculated requirements from the actual intakes. According to data previously obtained in our experimental herd, the predicted energy deficiency for the 13AL sows was approximately 20% of the energy requirements. Feed restriction should have resulted in a similar energy deficiency in the 7R sows. Feed allowance to these sows was based a priori on the usual average feed intake of primiparous sows and the average litter growth rate in the herd. The amounts of feed provided each week were corrected on the basis of estimated energy balance of the 13AL and 7R sows.
The body chemical composition on d 1 and 29 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), and protein (kg) = 2.28 + (0.178 x EBW) – (0.333 x P2), where EBW (kg) is the sow empty live weight estimated from the live weight (EBW = 0.905 x BW1.013), and P2 is the backfat thickness (mm) at the P2 level.
Profiles of plasma glucose and insulin during the glucose tolerance tests were described through various parameters: for each tolerance test, the mean fasting (or basal) levels of glucose and insulin, corresponding to the means of the –15 and –2 min values, were calculated. Glucose half-life was estimated from individual regression equations relating the logarithm of glucose level to the time between time 0 and time when the concentration passes through the fasting level on the way down. Glucose half-life was calculated as the time at which the glucose levels reached 50% of the peak levels. The time required to return to this basal level was also determined for glucose by interpolation. The area under the insulin curve (AUC) was calculated by linear interpolation of insulin levels between the measurements and with the fasting insulin level as the basal line. This estimation was made between time 0 and the time when the insulin levels returned to the fasting level. The time required to reach 50% of this area was also determined by interpolation.
Sows were classified into 3 scores of ovarian activity based on the number of growing follicles and follicular diam.: score 1 for poorly-developed ovaries, score 2 for intermediate ovaries, and score 3 for well-developed ovaries, with average diam. of the largest 14 follicles being less than 6 mm, between 6 and 7 mm, and more than 7 mm, respectively.
Data were analyzed by analysis of variance using the GLM procedure (SAS Inst. Inc., Cary, NC). Models included the effects of treatment and replicate and the interaction between these 2 factors. When the treatment effect was significant, means of the 3 groups were separated by F-protected LSD. For metabolites and hormones, a split-plot design was used, with treatment, replicate, sow nested within group (error to test the effects of treatment, replicate, and the interaction), day of sampling, and the interactions. Further analyses were done within day of lactation (treatment effect) and within sows’ group (day of lactation effect). An analysis of variance was done with ovarian score as a main factor. Correlations between reproductive characteristics and sow endocrine and metabolic status were evaluated by using the Pearson coefficient. For discontinuous variables (number of LH pulses and ovarian score), however, the Spearman coefficient was used. In the results, the means and the SEM are given.
Twenty-eight lactating sows were initially allocated to the experimental treatments. One sow was withdrawn from the study because of an aggressive behavior, and another one died. Five sows were removed from the calculations because of low piglet growth (<150 g/d in the 13AL group and <200 g/d in the 7AL and 7R groups).
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RESULTS
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Sow and Litter Performance
Litters of 13 or 14 piglets had a greater (P < 0.05) daily growth rate than litters of 7 piglets, whereas growth rate did not differ between the 2 groups of sows nursing 7 piglets (Table 2). In all groups of sows, growth rate was lower (P < 0.05) during the first week of lactation than during the next 3 wk. Average piglet growth rate was lower (P < 0.05) for the 13AL than for the 7R sows and intermediate for the 7AL sows.
During lactation, the 13AL sows ate more feed than the 7R sows (P < 0.05) but not more than the 7AL sows (P > 0.1; Table 3). Sows in the 7AL group lost no or little BW, backfat, and estimated body reserves (Table 4). Their energy balance over the whole lactation was nearly nil (94% of total energy requirements). The energy balance of the 13AL and 7R sows was negative and averaged 79% of requirements. Losses of backfat and estimated lipid content did not differ between the 13AL and 7R sows (P > 0.1). Losses of BW and estimated body protein were greater (P < 0.05) in the 13AL than in the 7AL sows and intermediate in the 7R sows (Table 4).
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Table 4. Variations in BW, backfat thickness, and estimated body lipid and protein content of sows during lactation1
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Sow Metabolism
There was an interaction (P < 0.05) between treatment and day of sampling for plasma IGF-I. Concentrations of IGF-I were lower in the 13AL than in the 7AL and the 7R sows on d 15 and 29 of lactation (Figure 1), whereas no differences were observed between the 3 groups 3 d after weaning.
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Figure 1. Plasma concentrations of IGF-I on d 15 and 29 of lactation and 3 d after weaning (means ± SEM) in sows with 13 or 14 piglets and fed ad libitum (13AL), sows with 7 piglets and fed ad libitum (7AL), and sows with 7 piglets and fed a restricted diet to mimic the energy deficiency of the 13AL sows (7R). a,bWithin day of lactation, significant differences between groups (P < 0.05).
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Glucose Tolerance Tests.
Fasting concentrations of insulin and glucose were not influenced by treatments or stage of lactation (Table 5). Profiles of glucose and insulin during glucose tolerance tests are presented in Figure 2. Glucose half-life and time needed for insulin to reach 50% of the area under the curve were longer on d 16 than on 27 of lactation (22.5 ± 1.1 vs. 18.8 ± 0.9 min; P = 0.03 and 20.2 ± 0.9 vs. 18.2 ± 0.7 min; P = 0.05, respectively). An overall treatment effect was also found: insulin AUC was greater in 7AL than in the 13AL sows (3.97 ± 0.68 vs. 2.39 ± 0.25 mIU·mL–1·min–1, P = 0.08) and intermediate in the 7R group (3.22 ± 0.41 mIU·mL–1·min–1), whereas glucose half-life and time needed for glucose to return to basal level did not differ between groups of sows.
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Table 5. Fasting concentrations of glucose, insulin, and NEFA, and characteristics of glucose and insulin profiles of sows during glucose tolerance tests1
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Figure 2. Plasma glucose and insulin concentrations during the glucose tolerance test according to the day of lactation (A) and the treatment group (B; means ± SEM) in sows with 13 or 14 piglets and fed ad libitum (13AL), sows with 7 piglets and fed ad libitum (7AL), and sows with 7 piglets and fed a restricted diet to mimic the energy deficiency of the 13AL sows (7R). Glucose half-life was 22.5 ± 1.1 on d 16 vs. 18.8 ± 0.9 min on d 27 (P = 0.03). Insulin AUC was 3.97 ± 0.68, 3.22 ± 0.41, and 2.39 ± 0.25 mIU·mL–1·min in the 7AL, 7R, and 13AL sows, respectively (7AL vs. 13AL, P = 0.08).
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Profile analyses were further detailed within day of lactation and within group of sows. On d 16, none of the variables describing the glucose and insulin profiles were influenced by treatments (Table 5
). Fasting concentrations of NEFA were less in the 7AL than in the 13AL sows (P < 0.06) and intermediate in the 7R sows. On d 27, glucose profiles did not differ between the 3 groups of sows, whereas insulin profiles did (Table 5). Insulin AUC was greater (P = 0.08) in the 7AL than in the 13AL sows and intermediate in the 7R sows. The time needed to reach 50% of the area under the curve was longer in the 7AL sows than in the 2 other groups of sows (P = 0.03). Profiles of insulin and glucose varied during lactation in the 13AL and the 7R sows but not in the 7AL sows (Table 5). In the 13AL group, glucose half-life (P = 0.09), insulin AUC (P = 0.06), and fasting concentrations of NEFA (P = 0.04) decreased between d 16 and 27 of lactation. In the 7R sows also, glucose half-life (P = 0.01), insulin AUC (P = 0.05), and time needed to reach 50% of this area (P = 0.01) decreased (Table 5).
Reproductive Data
Three days after weaning, the number of large follicles in the ovaries did not differ between the 3 groups of sows (Table 6). Values were then compared according to litter size (13 vs. 7 piglets). The volume of the largest follicle and the average volume of the largest 14 follicles were lower in sows nursing 13 or 14 piglets than in sows nursing 7 piglets (140 ± 28 vs. 190 ± 22 µL, P = 0.06 and 95 ± 20 vs. 140 ± 14 µL, P = 0.04, respectively). Mean and basal concentrations of LH in plasma were greater in late lactation (d 29) than in midlactation (d 15; Table 7). Pulse frequency was not influenced by the day of sampling.
Criteria of follicular development after weaning were highly correlated with the frequency of LH pulses and mean concentration of LH measured in midlactation but not in late lactation (Table 8).
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Table 8. Correlation coefficients between ovarian characteristics 3 d after weaning and LH secretion of sows in mid- or late lactation1,2
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Relationships Between Metabolic and Reproductive Variables
Ovarian score was correlated positively with sow BW at weaning (r = 0.62; P = 0.004), backfat depth (r = 0.47; P = 0.04) and estimated body lipid content (r = 0.65; P = 0.002) at weaning and losses during lactation (back-fat: r = 0.58; P = 0.009; lipid: r = 0.53; P = 0.02). Relationships with estimated body protein content and losses during lactation were not significant. Ovarian score was also positively correlated with IGF-I concentrations at d 15 (r = 0.49; P = 0.03) and 29 (r = 0.57; P = 0.01).
No relationships were found between ovarian score and glucose half-life or time needed for glucose to return to basal level in mid- or late lactation. Ovarian score was correlated with the time needed to reach 50% of insulin AUC (r = 0.52; P = 0.02) but not with insulin AUC (r = 0.24; P = 0.32) measured in midlactation. Ovarian score was correlated with insulin AUC (r = 0.56; P = 0.01) and the time needed to reach 50% of the insulin curve (r = 0.74; P = 0.001) measured at d 29 of lactation. Glucose and insulin profiles in late lactation are presented according to sow ovarian score (Figure 3).
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Figure 3. Plasma glucose (A) and insulin (B) concentrations during the glucose tolerance test on d 29 of lactation according to the ovarian score (means ± SEM); score 1 = poorly developed ovaries; score 2 = intermediate ovaries; score 3 = well-developed ovaries.
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DISCUSSION
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Experimental Design
The present experiment was designed to investigate the respective influence of suckling intensity and energy deficiency on the reproductive axis in primiparous sows. Our experimental objective was therefore to compare 3 groups of sows, 2 groups nursing a large or a small litter and having a similar energy deficiency, and a group of sows nursing a small litter and without energy deficiency. To meet this objective, we had to eliminate 5 out of 26 sows from the analysis. These sows were poor milk producers and had an energy balance either nil (three 13AL sows) or highly positive (two 7AL sows). This illustrates that lactational ability greatly varies between individual sows. As a consequence, only 21 sows were available in the experiment. Sows in the 7AL group lost no or little body reserves, and their energy balance was nearly nil. The 13AL and 7R sows exhibited similar relative negative energy balance, but the absolute deficit was greater in the 13AL sows. Because losses of backfat thickness and estimated lipid content were similar in the 2 groups, we could have expected a greater protein mobilization in the 13AL sows. Kim and Easter (2001) reported a linear increase in protein mobilization as litter size increased, in primiparous sows fed 4 kg of feed daily. In our experiment, the lower concentrations of IGF-I also supported a greater mobilization of body protein in the 13AL than in the 7R sows. The estimated protein loss (–2.6 vs. –0.9 kg in the 13AL and the 7R groups, respectively) did, however, not differ significantly.
Litter Growth and Milk Production
As expected, growth rate of large litters was greater than that of litters with fewer piglets, which reflects a greater milk production by sows nursing 13 or 14 piglets. The positive relationship between litter size and milk yield was previously described (Elsley, 1971; King et al., 1989; Auldist et al., 1998). Increased feed intake is not always associated with increased litter size in sows (Eissen et al., 2003). Even when it is the case, extra feed intake is generally insufficient to meet higher needs, which results in higher BW loss (Eissen et al., 2003). In the current study, feed intake did not differ between the sows fed ad libitum. As a consequence, the 13AL sows lost 28 and 8% of their initial lipid and protein content, respectively, whereas the 7AL lost very few body reserves. Maternal body reserve mobilization is likely to be stimulated by the endocrine consequences of intense suckling. Indeed, stimuli associated with suckling in sows induce the secretion of hormones involved in lactogenesis (prolactin, growth hormone, cortisol) and milk ejection (oxytocin), and metabolic adaptations that favor preferential drive of nutrients toward mammary glands (review: Quesnel and Prunier, 1995). Maternal mobilization of lipids is likely to be stimulated by GH that inhibits lipogenesis and by cortisol that stimulates lipolysis. Algers et al. (1991) reported that duration of teat massage positively influences prolactin and glucagon release and negatively influences somatostatin release. However, it is not known whether secretion of these hormones is influenced by the number of suckling piglets. Mobilization of maternal protein in the 13AL sows is likely to be facilitated by the reduction in circulating concentrations of IGF-I, itself related to the energy deficiency due to high milk production.
In addition, the development of peripheral insulin resistance, which favors glucose availability for uterus during pregnancy and mammary glands during lactation at the expense of muscles and adipose tissue, has been reported in many mammalian species. In sows, this resistance has been shown to develop during the third part of pregnancy and to increase further during lactation (Etienne and Père, 2002). Development of insulin resistance has been suggested to be induced by the elevated NEFA concentration in late pregnant rabbits (Gilbert et al., 1991, 1993). We hypothesized that the intensity in insulin resistance could be related to the amount of energetic substrates required by mammary glands and thus to litter size. However, comparison of the 3 groups of sows does not support this hypothesis. Glucose tolerance was not affected by litter size or by energy deficiency in midlactation. In late lactation, moreover, the greatest insulin response to glucose challenge was observed for the 7AL sows, whereas glucose half-life did not differ between the 3 groups. In these sows, therefore, insulin was less efficient to stimulate glucose uptake. Insulin resistance in the 13AL and the 7R sows decreased between d 16 and 27 of lactation. Reduction by at least 4 min of glucose half-life can be considered as physiologically relevant because a change of the same extent is observed between d 35 and 108 of gestation (Père et al., 2000). Whereas insulin resistance decreased during lactation in the 13AL and the 7R sows, it did not change in the 7AL. We suggest therefore that, independently of litter size, sows adapted glucose metabolism to their own nutrient intake and nutrient requirements for milk production. Indeed, the 7AL sows ate slightly less feed during the fourth week of lactation than during the third despite a sustained milk production, as illustrated by litter growth. This is in agreement with variations in NEFA; the 13AL and 7R sows had lower fasting concentrations of NEFA on d 27 than on d 16 of lactation, whereas these concentrations did not vary in the 7AL sows. Therefore, increase in milk production as litter size increases is not necessarily associated with an accentuation of sow insulin resistance. More likely, each sow adapts its own insulin and glucose metabolism to nutrient balance throughout lactation.
Reproductive Performance
In the present experiment, sows that nursed 13 or 14 piglets had slightly less developed ovaries than sows with 7 piglets, whatever the nutrient balance of the latter sows. Based on follicular growth rate (+1 mm diam./d in late follicular phase, Morbeck et al., 1992), only a marginal delay of about 1 d in the return to estrus after weaning could be expected. One may wonder whether a longer delay could occur for sows prone to reproductive problems or reared in suboptimal conditions. This effect of litter size was not accompanied by differences in LH secretion, which agrees with the literature. Varley and Foxcroft (1990) suggested that the stimulation of follicular development is not necessarily associated with measurable changes in circulating LH.
Follicular development after weaning was highly variable between sows. To investigate the connection between follicular development, LH secretion, and glucose metabolism, further analyses were performed by correlation analyses and after categorizing sows according to ovarian score. Ovarian characteristics after weaning were related to LH secretion in midlactation on the one hand and to glucose metabolism in late lactation on the other hand. The latter result is, however, difficult to interpret. Good follicular development was associated with sustained secretion of insulin in response to glucose challenge, whereas glucose half-life did not differ between sows classified according to their follicular development. Considering these insulin and glucose profiles, more insulin is likely to be needed to stimulate glucose uptake by cells. We could therefore conclude that sows with the most active follicular growth are more resistant to insulin than more inhibited sows. At first sight, this seems to contrast with the literature because there is strong evidence of the stimulatory action of insulin on the activity of the gonadotropic axis (for reviews, see Cosgrove and Foxcroft, 1996; Monget and Martin, 1997; Cox, 1997). However, overall insulin sensitivity mainly results from sensitivity in muscles and adipose tissue, and results cannot be extrapolated to insulin sensitivity in the hypothalamus or ovaries. Alternatively, it is questionable whether the fact that circulating concentrations of insulin remain greater for a longer time may have positive effects on LH secretion, follicular growth, or both. In women, various syndromes of insulin resistance were associated with ovarian hyperstimulation by insulin (Porestky and Kalin, 1987). These authors suggested that the high quantity of insulin binds to ovarian insulin and IGF-I receptors and acts in synergy with gonadotropins to stimulate follicular maturation.
Finally, our results indicate that ovarian development was not only related to BW loss during lactation but also to the amount of body reserves at weaning. This agrees with previous findings showing that large body reserves at farrowing may attenuate the negative impact of a nutrient deficiency during lactation on post-weaning performance of primiparous sows (Mullan and Williams, 1989; Clowes et al., 2003; Quesnel et al., 2005). Considering correlations, lipid metabolism seems to be more critical than protein loss, in regard to ovarian score. However, the role of lean reserves in the interactions between metabolic status and reproduction has also been described (Williams, 1998; Clowes et al., 2003; Quesnel et al., 2005).
In conclusion, primiparous sows nursing 13 or 14 piglets had to mobilize body reserves to support large litter growth. The great milk yield involves endocrine and metabolic adaptations, amongst which increased insulin resistance seems not to be involved. They exhibit slightly altered or delayed follicular development after weaning in comparison with sows nursing 7 piglets. Besides litter size influence, our results point out that, for each sow, metabolic status is adapted throughout lactation in response to interactions among body reserves, nutrient intake, and nutrient needs, and that metabolic status may influence ovarian activity after weaning.
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IMPLICATIONS
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In the context of increasing sow prolificacy, producers could be tempted to keep a maximum of piglets with their dam, even with primiparous sows, to limit crossfostering and use of nursing sows. Besides, nursing a large litter during the first lactation is sometimes believed in practice to stimulate teat development and milk production for subsequent lactations. Findings from the current study indicate that nursing a large litter increases sows’ weight loss during lactation. Consequences on the reproductive axis are moderate in our experimental conditions.
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Footnotes
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1 The authors wish to acknowledge Y. Lebreton, M. Massard, L. Gaillard, M. Lefebvre, and B. Trépier for surgical assistance, animal care, and help for collection of blood samples. They are grateful to C. David, A. Pasquier, and A. M. Mounier for expert technical assistance. They also thank Y. Combarnous (INRA/CNRS/Univ. Tours, Nouzilly, France) for gift of highly purified porcine LH for iodination, and I. Louveau (INRA Saint-Gilles, France) and U. Weiler (University of Hohenheim, Germany) for providing antiserum against IGF-I. 
2 Corresponding author: Helene.Quesnel{at}rennes.inra.fr
Received for publication March 20, 2006.
Accepted for publication August 8, 2006.
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LITERATURE CITED
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Abstract
INTRODUCTION
