Impact of diet deprivation and subsequent overallowance during gestation on mammary gland development and lactation performance C. Farmer, M.-F. Palin and Y. Martel-Kennes J ANIM SCI 2014, 92:141-151. doi: 10.2527/jas.2013-6558 originally published online December 18, 2013

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Impact of diet deprivation and subsequent overallowance during gestation on mammary gland development and lactation performance1 C. Farmer,*2 M.-F. Palin,* and Y. Martel-Kennes† *Agriculture and Agri-Food Canada, Dairy and Swine R and D Centre, Sherbrooke, QC J1M 1C8, Canada; and †La COOP Fédérée, Animal Nutrition Division, St-Romuald, QC G6W 5M6, Canada

ABSTRACT: The impacts of diet deprivation and subsequent overallowance during gestation on mammary gene expression and development and lactation performance were determined. Gilts were reared under a conventional (control, CTL; n = 59) or an experimental (treatment, TRT; n = 56) dietary regimen during gestation. The experimental regimen provided 70% (restriction diet, RES) and 115% (overallowance diet, OVER) of the protein and DE contents provided by the CTL diet. The RES diet was given during the first 10 wk of gestation followed by the OVER diet until farrowing. Some gilts (14 CTL and 14 TRT) were slaughtered on d 110 of gestation, and the others were allowed to farrow. Of these remaining sows, 28 (14 CTL and 14 TRT) were slaughtered on d 21 of lactation, and the rest underwent a second lactation. At each slaughter, mammary tissue was collected for compositional analyses and assessment of gene expression. Milk samples were collected on d 17 of the first lactation. Litter size was standardized to 11 ± 1, and piglets were weighed weekly until d 18 in both parities. The BW and back fat thickness of TRT first-parity sows were less than those of CTL sows in gestation (P < 0.05), and their BW was also less

in lactation (P < 0.05). The BW of TRT second-parity sows was still less at mating (P < 0.05) and tended to be less on d 1 of lactation (P < 0.10) compared with CTL sows. There were no differences in piglet growth between CTL and TRT litters in either parity, yet mammary development and mammary gene expression were affected by treatment. There was less parenchymal tissue (P < 0.01) at the end of the first gestation in TRT than in CTL sows, but parenchymal tissue composition was not altered by treatment. Relative abundance of IGF-1 (P < 0.05), ornithine decarboxylase (P < 0.05), signal transducer and activator of transcription 5B (P < 0.05), and whey acidic protein (WAP, P < 0.01) genes in parenchyma at the end of the first gestation was lower in TRT than in CTL sows, and the effect on WAP genes was still present at the end of the first lactation (P < 0.01). Mammary composition at the end of the first lactation and milk composition were unaffected by treatment. In conclusion, feed deprivation and subsequent overallowance in gestation had unfavorable effects on sow BW, back fat, mammary development, and mammary gene expression at the end of gestation, but piglet growth rate over the 2 parities was not affected.

Key words: diet deprivation, diet overallowance, gene expression, gestation, mammary development, sows © 2014 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2014.92:141–151 doi:10.2527/jas2013-6558 INTRODUCTION Growth rate of suckling piglets is largely determined by milk yield, yet sows cannot produce enough 1The

authors thank L. Thibault, A. Bernier, D. Beaudry, and L. Marier for their invaluable technical assistance, the staff at the CRF research farm, especially I. Cormier, for carrying out the project, the staff of the Swine Complex for care and slaughter of animals, and S. Méthot for statistical analyses. Sincere thanks are extended to La COOP Fédérée (St-Romuald, QC, Canada) for financial and technical support. 2Corresponding author: [email protected] Received April 8, 2013. Accepted November 4, 2013.

milk to sustain optimal growth of their litter (Harrell et al., 1993). Considering that the number of mammary secretory cells at the onset of lactation has an impact on sow milk yield (Head and Williams, 1991) and that rapid mammary accretion occurs in the last third of gestation (Sorensen et al., 2002), it would be of interest to develop feeding strategies to stimulate mammary development in late gestation. Overfeeding a sow during gestation negatively affects mammary development (Head and Williams, 1991), and feed restriction during prepuberty also reduces mammary tissue (Farmer et al., 2004). The use of compensatory

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feeding regimens to stimulate mammary development and lactation potential was studied in rodents. A stairstep nutrition model inducing compensatory growth during peripuberty and gestation improved subsequent lactation performance of rats by modulating mammary cell differentiation and increasing casein β (CSN2; Moon and Park, 2002) and ornithine decarboxylase (ODC1; Kim et al., 1998) mRNA levels in mammary tissues. In swine, Crenshaw et al. (1989) reported that diet deprivation followed by overallowance during the growing, finishing, and gestation phases increased sow milk yield and stimulated the relative expression of CSN2 in mammary tissue. It was recently demonstrated that using the same feeding regimen only in the growing-finishing period had no beneficial effect on mammary development at puberty (Lyvers-Peffer and Rozeboom, 2001; Farmer et al., 2012a) or at the end of gestation (Farmer et al., 2012b). This indicates that the gestation period could be the most sensitive physiological state to stimulate mammogenesis. It was therefore hypothesized that diet deprivation and overallowance during gestation could affect mammary development and mammary gene expression at the end of the first gestation or lactation, thereby improving subsequent milk yield. MATERIALS AND METHODS Animals were cared for according to a recommended code of practice (Agriculture and Agri-Food Canada, 1993), and procedures were approved by the Institutional Animal Care Committee of the Dairy and Swine Research and Development Centre of Agriculture and Agri-Food Canada in Sherbrooke. Animals and Treatments One hundred and thirty-six Yorkshire × Landrace gilts were bred via AI using pools of semen from 50 Duroc boars of proven fertility. Gestating gilts were then fed a conventional (control, CTL; n = 59) or an experimental (treatment, TRT; n = 56) dietary regimen. The TRT regimen was designed to restrict growth and then induce compensatory growth by providing 70% (restriction diet, RES) and 115% (overallowance diet, OVER), respectively, of the CP and DE contents provided by the CTL diet. The RES diet (2.27 kg/d) was given for 10 wk starting at mating followed by the OVER diet (2.27 kg/d) until farrowing. These diets are described in Table 1. Representative feed samples were taken at manufacturing of each new batch throughout the experiment for compositional analyses (Table 1). Gilts were housed in individual gestation pens (1.5 × 2.4 m). Twenty-eight gilts (14 CTL and 14 TRT) were weighed and had their back fat thickness measured ultrasonically (Vetkoplus,

Table 1. Composition of the experimental and lactation (LACT) diets (as-fed basis)1 Item CTL RES OVER LACT Ingredient, g/kg Corn 488.8 — 533.5 590.1 Wheat, soft 100.0 278.1 100.0 100.0 Wheat middlings 179.6 249.6 145.4 — Soybean meal (48% CP) 103.8 — 159.2 232.8 Oat hulls 100.1 442.6 — — Oat — — — 35.6 Animal fat — — 34.0 — Ground limestone 12.5 12.5 12.4 12.6 Monocalcium phosphate 4.4 3.8 4.6 13.7 NaCl 7.5 7.2 7.5 7.4 Lys∙HCl — 1.5 — 2.1 Met — 0.6 — 0.9 l-Thr — 0.7 — 0.9 Choline (60%) 0.70 0.72 0.70 1.15 Trace mineral and vitamin premix2 2.5 2.5 2.5 2.5 0.15 0.15 0.15 0.15 Phytase3 Calculated composition DE, kcal/kg 3,170 2,510 3,515 3,380 CP, % 13.00 9.12 14.95 17.36 Fat, % 3.06 2.02 6.28 2.82 Crude fiber, % 5.90 16.31 3.27 2.95 Total Lys, % 0.58 0.46 0.73 1.05 Ca, % 0.65 0.65 0.65 0.81 P, % 0.51 0.50 0.51 0.64 Met, % 0.23 0.21 0.26 0.37 Met + Cys, % 0.48 0.39 0.53 0.66 Analyzed composition CP, % 13.90 11.85 16.00 17.99 Ca, % 0.68 0.81 0.64 0.76 P, % 0.54 0.62 0.56 0.62 Na, % 0.31 0.32 0.32 0.30 Mg, % 0.19 0.24 0.19 0.15 1Control (CTL), restriction (RES), and overallowance (OVER) diets fed during gestation. The RES diet provided 70% and the OVER diet 115% of the CTL diet in the CP and DE contents. The RES diet was fed for the first 10 wk of gestation followed by the OVER diet for the remainder of gestation. 2Provided the following per kilogram of diet: Cu (copper sulfate), 40 mg; Zn (zinc sulfate), 160 mg; Se (sodium selenite), 0.3 mg; Mn (manganous sulfate), 80 mg; Fe (ferrous sulfate), 225 mg; I (ethylene diamine dihydroiodine), 1.5 mg; vitamin A, 15,000 IU; vitamin D, 1,300 IU; vitamin E, 65 IU; vitamin K, 50 mg; vitamin B12, 200 µg; thiamin, 1.2 mg; riboflavin, 4 mg; pantothenic acid, 12 mg; niacin, 10 mg; folate, 5 mg; biotin, 1.5 mg; and pyridoxine, 1.12 mg. 3Natuphos 5000 (BASF Corporation, North Mount Olive, NJ).

NOVEKO, Lachine, QC, Canada) at P2 of the last rib at mating and on d 70 and 108 of gestation. Jugular blood samples were obtained from these 28 gilts on d 70 and 108 of gestation, and they were then slaughtered on d 110 of gestation to obtain mammary glands for compositional analyses and samples of parenchymal tissue for gene expression analyses. Their uteri were removed, and fetuses were counted; ovaries were also obtained and weighed, and the number of corpora lutea was counted.

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The remaining gilts (45 CTL and 42 TRT) were allowed to farrow. They were fed a commercial lactation diet (Table 1) in 2 equal meals at a rate of 1.81 kg/d on the day of farrowing, 2.72 kg/d on d 1, 4.08 kg/d on d 2, 5.90 kg/d on d 3, 7.71 kg/d on d 4, and then ad libitum for the remainder of lactation. They had their back fat thickness measured ultrasonically at P2 of the last rib at mating and on d 1 and 17 of lactation. Sows were also weighed on d 1 and 17 of lactation. Litter size was recorded at birth and was standardized to 11 ± 1 piglets (within treatment group) within 24 h of birth, and piglets were weighed at birth, 24 h postpartum (after standardization of litter size), and on d 7, 14, and 18 of lactation. Piglets had no access to dry feed while suckling so that their weight gain provided an estimate of milk yield. Mortality rate was recorded. Piglets were weaned at d 19, and postweaning growth performance was evaluated using 6 pens of 14 pigs each for each treatment group. Weights of piglets were recorded at weaning and on d 49 postweaning. Jugular blood samples were obtained from 28 (14 CTL and 14 TRT) of these 87 gilts on d 70 and 108 of gestation and d 3 and 17 of lactation. Representative milk samples were obtained from 40 (20 CTL and 20 TRT) of the 87 gilts on d 17 of lactation by collecting milk from 3 functional glands (anterior, middle, and posterior) encompassing both sides of the udder after an intravenous injection of 1.0 mL of oxytocin (20 IU/mL; P.V.U., Victoriaville, QC, Canada) was given. Piglets were separated from their dam for 45 min before oxytocin was injected. Twenty-eight sows (14 CTL and 14 TRT) were slaughtered on d 18, 19, or 20 of lactation (weaning) to obtain mammary glands for compositional analyses and samples of parenchymal tissue for gene expression analyses. The postweaning interval to estrus was noted on the rest of the sows (31 CTL and 28 TRT), which were allowed to farrow a second time. Their BW, back fat thickness and feed intakes were recorded, and litter size and weights of piglets were recorded similarly to the first lactation, with the omission of the BW on d 14 of lactation. The experiment took place between October 2010 and January 2012. Blood Handling and Assays Blood samples collected in gestation or lactation were used to measure concentrations of urea, FFA, glucose, IGF-1, and prolactin. Samples collected on d 110 of gestation were also assayed for progesterone. Blood sampling was done between 0800 and 1000 h. Blood samples were collected in EDTA tubes (Becton Dickinson and Co., Rutherford, NJ), except those for glucose analyses, which were collected into tubes containing 10.0 mg of potassium oxalate and 12.5 mg of sodium fluoride to inhibit glycolysis. All samples were put on ice and centrifuged within

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20 min at 1800 × g for 12 min at 4°C, and plasma was immediately recovered and frozen at –20°C until assayed. Concentrations of IGF-1 were measured with a commercial kit for humans (ALPCO 26-G; ALPCO Diagnostics, Salem, NH), with small modifications as detailed previously (Plante et al., 2011). Validation for a plasma pool from sows was conducted. Parallelism was 101.2%, and average mass recovery was 101.3%. Sensitivity of the assay was 0.10 ng/mL. The intra- and interassay CV were 3.77% and 4.62%, respectively. Concentrations of prolactin were determined according to a previously described RIA (Robert et al., 1989). The radioinert prolactin and the first antibody to prolactin were purchased (A. F. Parlow; U.S. National Hormone and Pituitary Program, National Institute of Diabetes and Digestive and Kidney Diseases, Torrence, CA). Validation for a plasma pool from lactating sows was conducted. Parallelism was 95.6%, and average mass recovery was 98.9%. The sensitivity of the prolactin assay was 1.5 ng/mL. The intra- and interassay CV were 3.50% and 5.04%, respectively. Progesterone was measured with commercial kits (Progesterone CT; ICN Pharmaceuticals Inc., Costa Mesa, CA). Intra- and interassay CV were 4.18% and 7.85%, respectively. Glucose was measured by an enzymatic colorimetric method with a commercial kit (Boehringer Mannheim, Laval, QC, Canada). Intra- and interassay CV were 1.57% and 1.85%, respectively. Urea was measured by colorimetric analysis using an autoanalyzer (Auto-Analyser 3; Technicon Instruments Inc., Tarrytown, NY) according to the method of Huntington (1984). Intra- and interassay CV were 1.60% and 1.81%, respectively. Concentrations of FFA were also measured by colorimetry with a commercial kit (Wako, Richmond, VA). Intra- and interassay CV were 2.05% and 5.99%, respectively. Milk Composition Whole milk was analyzed for DM, protein, fat, and lactose contents. Dry matter was measured according to a validated method using forced-air oven drying (AOAC, 2005). Protein content was determined in duplicates with the micro-Kjeldahl method (Kjeltec Auto System; Tecator AB, Hoganas, Sweden), and fat was extracted using an established ether extraction method (AOAC, 2005). Lactose was measured by a colorimetric method using a commercial kit (Megazyme International Ireland Ltd., Bray, Co. Wicklow, Ireland). Intra- and interassay CV were 1.04% and 1.58%, respectively. Protein Quantification for Milk Casein Beta and Whey Acidic Protein Milk samples (200 μL) were centrifuged at 5000 × g for 15 min at room temperature, and the aqueous phase

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(skim milk) was collected and conserved at –20°C until used for protein quantification. Casein β and whey acidic protein (WAP) protein quantifications were performed using dot blot analyses as previously described (Farmer et al., 2012b). Mammary Gland Measurements At slaughter, mammary glands (functional glands only on d 21 of lactation) from 1 side of the abdominal wall were excised and were stored at –20°C until dissection and analyses for tissue composition. Frozen mammary glands were trimmed of skin and teats and subsequently stored at –20°C. They were then cut into 2-cm slices, and mammary parenchymal tissue from each slice was dissected from surrounding adipose tissue (i.e., extraparenchymal tissue) at 4°C and both parenchymal and extraparenchymal tissue weights were recorded. Parenchymal tissue from all dissected and sliced glands was homogenized, and a representative sample was used for determination of composition by chemical analysis. The RNA content of parenchymal tissue was measured by ultraviolet (Volkin and Cohn, 1954), and the DNA content of parenchymal tissue was evaluated in all samples using a method based on fluorescence of a DNA stain (Labarca and Paigen, 1980). Dry matter, protein, and lipid contents were also determined (AOAC, 2005) in parenchyma. Parenchymal tissue samples were collected for measurement of the relative mRNA abundance for IGF-1, the long form of the prolactin receptor (PRLR-LF), signal transducers and activators of transcription 5A (STAT5A), STAT5B, STAT3, WAP, CSN2, γ-glutamyltransferase 1 (GGT1), caspase 3 (CASP3), and ODC1. These samples were frozen immediately in liquid nitrogen and stored at –80°C. Immunohistochemistry Parenchymal tissue samples (approximately 50 mg) were collected at slaughter from 5 to 7 sows from each treatment and were fixed overnight in 4% (w/v) neutral buffered paraformaldehyde. Tissue samples were then dehydrated in a series of graded ethanol baths and embedded in paraffin, and 4-µm-thick sections were cut using a microtome. Proliferating mammary cells were quantified in mammary parenchyma collected on d 110 of gestation and d 19 of lactation, using a mouse anti-Ki-67 antibody and a detection system [Histostain-Plus (DAB, Broad Spectrum), LAB-SA; Invitrogen, Burlington, ON, Canada). Mammary cell apoptosis was quantified in parenchymal tissue collected on d 19 of lactation, using the terminal deoxynucleotidyl transferase dUTP nick-end labeling (TUNEL) assay with a colorimetric system (TUNEL System; Promega, Madison, WI). The manufacturer’s instructions were followed. Cells were counterstained with a

hematoxylin solution and then viewed with a microscope (Eclipse 50i Microscope; Nikon, Tokyo, Japan) fitted with a digital camera (QImaging Go-3; QImaging, Surrey, BC, Canada). At least 2,000 mammary cells were counted from 10 random fields within the same section using the ImageJ software, a Java-based image processing program (National Institutes of Health, Bethesda, MD). Cell counts were performed in 2 different tissue sections (duplicates). Caspase-3 was also measured in parenchymal tissue collected on d 19 of lactation to assess mammary cell apoptosis. Cells expressing the caspase-3 protein were identified using a recombinant rabbit monoclonal antibody (CASP3[D175], ABfinity; Invitrogen) and a detection system (Histostain-Plus [DAB], Broad Spectrum, LAB-SA; Invitrogen, Burlington, ON, Canada). Cell proliferation and apoptosis were expressed as the percentage of total counted cells for the Ki-67 assay (proliferation) and for the caspase-3 and TUNEL assays (apoptosis). RNA Extraction, Complementary DNA Synthesis, and Real-Time PCR Amplifications of Studied Genes Total RNA was extracted from parenchymal tissue and reverse transcribed as previously described (Labrecque et al., 2009). Integrity and purity of extracted RNA were assessed using a spectrophotometer (NanoDrop ND-1000; NanoDrop Technologies Inc., Wilmington, DE). The relative mRNA abundance of studied genes (CASP3, CSN2, GGT1, IGF1, ODC1, PRLR-LF, STAT3, STAT5A, STAT5B, and WAP) was determined using realtime PCR amplifications. Primers were designed using the software (Primer Express Software 3.0; PE Applied BioSystems, Foster City, CA). For the CSN2, GGT1, IGF1, ODC1, PRLR-LF, STAT5A, STAT5B, and WAP genes, the description of primer sequences, GenBank accession numbers, and amplified product size were reported previously (Farmer et al., 2012a). For the CASP3 gene, forward 5′-TGAGGCAGACTTCTTGTATGCATAT-3′ and reverse 5′-TTCAGCGCTGCACAAAGTG-3′ primers (NM_214131.1, 105 bp amplicon) were used. For the STAT3 gene, the following primer pair was used: forward 5′-ACCAACACGAAAGTGATGAATATGG-3′ and reverse 5′-TCTCTCAGGGTCAGGTGTTTGA-3′ (NM_001044580, 80 bp amplicon). The PCR amplifications were performed in a 10-μL reaction volume consisting of forward and reverse primers (concentrations ranging from 150 to 900 nM), 5 μL of 2 × Power SYBRGreen Master Mix (PE Applied BioSystems), 3 μL of 15 × diluted cDNA, and 0.05 μL of uracil N-glycosylase AmpErase (PE Applied BioSystems). Cycling conditions, detection, and data analysis were performed as previously described (Labrecque et al., 2009). Specificity of amplified fragments was verified with the melting curve analysis software (Dissociation Curves v1.0; PE Applied BioSystems).

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Four reference genes were amplified to identify those that were the least affected by treatments. These reference genes are peptidylprolyl isomerase A (PPIA), actin β (ACTB), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), and ubiquitin C (UBC). Primer pairs, GenBank accession numbers, and amplified products size were previously described for PPIA, GAPDH, and UBC (Farmer et al., 2012a). For ACTB, the following primer pair was used: forward 5′-CATCACCATCGGCAACGA-3′ and reverse 5′-GGATGTCGACGTCGCACTT-3′ (XM_003124280, 128 bp amplicon). Amplifications were performed in triplicate and standard curves were established in duplicate for each gene. Standard curves were composed of serial dilutions of complementary DNA pools (Labrecque et al., 2009) and were used to obtain the relative quantification of mRNA using the standard curve method as described (Applied Biosystems, 1997). Relative quantification values were then obtained using a normalization factor calculated with a combination of the ACTB and cyclophilin A (CYCLO) reference genes in gestation and the CYCLO and GAPDH genes in lactation. The normalization factor was calculated with the geNorm algorithm, which uses the geometric mean of a user-defined number of reference genes (Andersen et al., 2004). For each experimental sample, the amount of the studied genes relative to the reference genes mRNA was determined from their respective standard curves. Relative quantity ratios were obtained by dividing the relative quantity units of the studied genes by those of the reference genes. Mean values from triplicates were used to perform the statistical analyses.

Table 2. Weight, back fat thickness, and lactation feed intakes of first-parity sows [59 control (CTL) and 56 treatment (TRT) sows in gestation and 45 CTL and 42 TRT sows in lactation]1 Groups Item BW, kg Mating d 70 of gestation d 108 of gestation Gain, mating to d 70 Gain, mating to d 108 Gain, d 70 to 108 d 1 of lactation d 17 of lactation Loss from d 1 to 17 Back fat, mm Mating d 70 of gestation d 108 of gestation Gain, mating to d 70 Gain, mating to d 108 Gain, d 70 to 108 d 1 of lactation d 17 of lactation Loss from d 1 to 17 Average daily feed intake, kg wk 1 of lactation wk 2 of lactation wk 3 of lactation wk 1 to 3 of lactation

CTL

TRT

SEM2

155.1 188.6a 210.6a 33.5a 55.5a 22.0a 193.2a 182.8c 10.3

153.2 170.2b 197.7b 17.1b 44.6b 27.5b 183.9b 175.1d 8.8

1.8 1.7 1.8 1.2 1.6 0.8 1.9 2.3 1.5

17.0 18.5a 17.5c 1.5a 0.6a –1.0a 15.9e 13.9 2.1e

17.5 16.3b 16.1d –1.2b –1.4b –0.2b 14.7f 13.2 1.6f

0.5 0.5 0.4 0.2 0.3 0.2 0.5 0.5 0.2

3.94 5.46 5.76 5.02

4.10 5.60 6.13 5.21

0.79 1.36 1.66 0.15

a,bMeans

within a row with different superscripts differ (P < 0.01). within a row with different superscripts differ (P < 0.05). e,fMeans within a row with different superscripts tend to differ (P < 0.10). 1CTL = control and TRT = treatment regimen, which provided 70% (restriction) and 115% (overallowance) of the CTL diet in the CP and DE contents. The restriction diet was fed for the first 10 wk of gestation followed by the overallowance diet for the remainder of gestation. Sows were fed 2.27 kg/d throughout gestation, and there were no refusals. 2Maximum value. c,dMeans

Statistical Analyses The MIXED procedure of SAS (SAS Inst. Inc., Cary, NC) was used for statistical analyses. The univariate model used for sow back fat thickness and BW, milk composition, mammary gland composition, real-time PCR, dot blots, apoptosis, cell proliferation, litter size at birth, piglet BW, and hormonal and ovarian variables included the effect of treatment, with the residual error being the error term used to test the main effects of treatment. Repeated measures ANOVA with the factors treatment (the error term being sow within treatment) and week of lactation (the residual error being the error term) and the treatment × week interaction were also performed on piglet BW. The main effect of parity on piglet BW data was also analyzed. The slice option was then used to determine effects at each time. Data in tables are presented as least squares means ± maximal SEM. RESULTS Weight, back fat thickness, and feed intakes of sows in first parity are shown in Table 2. The BW were

similar for both groups at mating (P > 0.10) but were lower for TRT sows thereafter from d 70 of gestation until weaning at d 17 of lactation (P < 0.05). Gains in BW from mating to d 70 or 108 of gestation were lower for TRT than CTL sows (P < 0.01), but BW gain between d 70 and 108 of gestation was greater for TRT than CTL sows (P < 0.01). The BW loss during lactation did not differ between CTL and TRT sows (P > 0.10). Similar differences between treatments were observed in back fat thickness of sows, with the exception that back fat loss in lactation tended to be less for TRT than CTL sows (P < 0.10) and back fat thickness did not differ between the 2 groups on d 17 of lactation (P > 0.10). The CTL sows had an increase in back fat during gestation, whereas TRT sows had a loss in back fat in

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Table 3. Circulating concentrations of urea, FFA, glucose, IGF-1, and progesterone in late gestation and lactation [14 control (CTL) and 14 treatment (TRT) sows at mating, 28 CTL and 28 TRT sows in gestation, 14 CTL and 14 TRT sows in lactation]1 Groups Item Urea, mmol/L Mating d 70 of gestation d 108 of gestation d 3 of lactation d 17 of lactation FFA, µEq/L Mating d 70 of gestation d 108 of gestation d 3 of lactation d 17 of lactation Glucose, mmol/L Mating d 70 of gestation d 108 of gestation d 3 of lactation d 17 of lactation IGF-1, ng/mL Mating d 70 of gestation d 108 of gestation d 3 of lactation d 17 of lactation Progesterone, ng/mL d 70 of gestation d 108 of gestation

CTL

TRT

SEM2

6.98e 5.73 5.55e 5.39 10.89

6.12f 5.90 6.10f 6.27 11.75

0.35 0.20 0.23 0.47 0.59

181.4 180.3a 416.3c 271.7 245.8

219.1 327.9b 258.6d 245.1 159.2

22.0 19.1 48.1 37.7 42.3

3.69 3.53 3.47 4.37 4.23

3.67 3.56 3.56 4.47 4.59

96.0 54.4a 38.7 97.2 102.6

103.4 36.5b 37.7 98.5 104.5

6.6 2.1 1.7 8.6 10.5

14.7 10.7

15.1 11.6

0.6 0.5

0.10 0.09 0.09 0.13 0.26

a,bMeans

within a row with different superscripts differ (P < 0.01). within a row with different superscripts differ (P < 0.05). e,fMeans within a row with different superscripts tend to differ (P < 0.10). 1CTL = control and TRT = treatment regimen, which provided 70% (restriction) and 115% (overallowance) of the CTL diet in the CP and DE contents. The restriction diet was fed for the first 10 wk of gestation followed by the overallowance diet for the remainder of gestation. 2Maximum value. c,dMeans

that period. Average daily sow feed intake during lactation was not affected by treatment (P > 0.10) but was altered by week of lactation (P < 0.01), with values increasing as lactation advanced. Postweaning interval to estrus was not affected by treatment (P > 0.10), being 5.25 and 5.05 d for CTL and TRT sows, respectively. Circulating concentrations of metabolites and hormones in first-parity sows are shown in Table 3. Urea tended to be greater in TRT than CTL sows on d 108 of gestation (P < 0.10), and concentrations of FFA were greater on d 70 of gestation (P < 0.01) and lower on d 108 of gestation (P < 0.05) in TRT than in CTL sows. Concentrations of IGF-1 were lower in TRT than in CTL

sows on d 70 of gestation (P < 0.001). Concentrations of glucose and progesterone were similar on all sampling days for CTL and TRT sows (P > 0.10). Mammary composition and relative mRNA abundance of selected genes in mammary tissue on d 110 of gestation are shown in Table 4. The number of teats was similar for sows from both treatment groups (7.60 and 7.77 [maximum SEM = 0.13] for CTL and TRT sows, respectively). The amount of parenchyma (whether total, per teat, or total corrected for BW at slaughter) was reduced in TRT sows compared with CTL sows (P < 0.05), and there was less total parenchymal fat (P < 0.01), protein (P < 0.01), DNA (P < 0.05), and RNA (P < 0.01) in TRT than in CTL sows, but there were no differences in the concentrations of these components (P > 0.10) in parenchymal tissue. There was also less total DNA (P < 0.05) and total RNA (P < 0.01) per teat in TRT than in CTL sows, and the RNA/ DNA ratio did not differ between groups (P > 0.10). There were differences in the relative abundance of mRNA for various genes in mammary parenchyma. Values for CSN2 were greater (P < 0.05) and those for IGF-1 (P < 0.05), ODC1 (P < 0.05), STAT5B (P < 0.05), and WAP (P < 0.01) were lower in parenchyma from TRT than from CTL sows. There were no differences between CTL and TRT sows for the percentage of proliferating mammary cells measured on d 110 of gestation (6.77% and 5.30% [maximal SEM = 0.96%] for CTL and TRT sows, respectively). At slaughter, the number of fetuses was similar in both groups (13.0 and 13.8 [maximal SEM = 0.5] for CTL and TRT sows, respectively). The number of corpora lutea (17.9 and 17.3 [maximal SEM = 0.8] for CTL and TRT sows, respectively) and weight of the ovaries (22.2 and 20.3 g [maximal SEM = 1.0 g] for CTL and TRT sows, respectively) were also unaffected by treatment (P > 0.10). In parity 1, litter size was similar for both treatments, being 12.16 and 12.15 for CTL and TRT sows, respectively (maximal SEM = 0.41; P > 0.10). There was a tendency for piglet birth weight to be lower in TRT than in CTL sows [1.32 vs. 1.41 kg (maximal SEM = 0.04 kg); P < 0.10]. Piglet mortality was minimal. Indeed, more than half the sows in the trial had no piglet mortality in the first 24 h postpartum. For parity 1, piglet mortality in the first 24 h postpartum was 3.3% ± 5.1% and 8.6% ± 11.2% (mean ± SD) for CTL and TRT litters, respectively, and from d 1 to 14 of lactation it was 4.5% ± 7.2% and 4.3% ± 4.8% (mean ± SD) for CTL and TRT litters, respectively. In parity 2, piglet mortality in the first 24 h postpartum was 3.3% ± 6.4% and 4.7% ± 8.5% (mean ± SD) for CTL and TRT litters, respectively, and from d 1 to 18 of lactation it was 5.5% ± 7.3% and 5.2% ± 6.7% (mean ± SD) for CTL and TRT litters, respectively. Piglet BW from sows of both parities are shown in Table 5. Statistical analyses, whether done separately on piglet BW for each day or on BW gain, showed no effect of treatment (P >

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Table 4. Mammary gland composition and relative mRNA abundance of selected genes on d 110 of gestation1 Item Extraparenchymal tissue, g Parenchymal tissue, g Parenchymal tissue/BW on d 108 of gestation, g Parenchymal tissue/teat, g Dry matter, % Fat,3 % Fat, g Protein,3 % Protein, g DNA,3 mg/g DNA, g total DNA/teat, g Protein/DNA RNA,3 mg/g RNA, g total RNA/teat, g RNA/DNA Mammary relative mRNA abundance4

Groups CTL TRT SEM2 1,048.4 883.2 106.2 1,617.2a 1,213.2b 97.9 7.76c 6.36d 0.47 213.3a 156.9b 12.9 39.1 38.5 1.05 63.3 62.9 1.7 398.5a 296.5b 25.3 34.1 34.6 1.6 212.8a 160.1b 13.7 5.76 6.17 0.25 3.63c 2.85d 0.26 0.48c 0.37d 0.03 59.8 55.9 2.3 7.82 8.12 0.33 4.91c 3.74d 0.33 0.48b 0.04 0.65a 1.37 1.36 0.08

CASP3 CSN2

0.818 0.154c

GGT1 IGF-1 ODC1 PRLR-LF STAT3 STAT5A STAT5B WAP

0.597 1.164c 1.188c 1.070 0.925 1.427 1.385c 0.011a

0.911

0.092

0.283d 0.502 0.956d 1.016d 1.196 0.784 1.253 1.152d 0.002b

0.030 0.052 0.058 0.056 0.114 0.057 0.106 0.083 0.001

a,bMeans

within a row with different superscripts differ (P < 0.01). within a row with different superscripts differ (P < 0.05). 1CTL = control (n = 15) and TRT = treatment regimen (n = 13), which provided 70% (restriction) and 115% (overallowance) of the CTL diet in the CP and DE contents. The restriction diet was fed for the first 10 wk of gestation followed by the overallowance diet for the remainder of gestation. 2Maximum value. 3Expressed on a dry matter basis. 4Relative mRNA abundances. Values correspond to the relative abundance of studied genes’ mRNA. CASP3, caspase 3; CSN2, casein beta; GGT1, gamma-glutamyltransferase 1; IGF-1, insulin-like growth factor 1; ODC1, ornithine decarboxylase 1; PRLR-LF, long form of the prolactin receptor; STAT3, STAT5A, and STAT5B, signal transducers and activators of transcription 3, 5A, and 5B; WAP, whey acidic protein. c,dMeans

0.10). The repeated measures in time analyses for piglet BW also showed no effect of treatment (P > 0.10) and no treatment × day interaction (P > 0.10), but there was an effect of day of lactation (P < 0.01). Milk composition on d 17 of lactation is shown in Table 6. There were no differences in DM, fat, protein, or lactose contents of milk from TRT and CTL sows (P > 0.10), but there were differences in contents of specific proteins. There was more milk casein-β (P < 0.01) and less WAP (P < 0.01) in milk from TRT than from CTL sows.

Table 5. Weight of piglets for 2 successive parities1 Groups Item Parity 1 BW, kg d 1 of lactation d 7 of lactation d 14 of lactation d 18 of lactation BW gain, kg d 1 to 18 Parity 2 BW, kg d 1 of lactation d 18 of lactation BW gain, kg d 1 to 18

CTL

TRT

SEM2

1.51 2.74 4.54 5.56

1.46 2.66 4.44 5.48

0.04 0.06 0.09 0.12

4.05

4.01

0.10

1.70 6.35

1.61 6.07

0.04 0.13

4.64

4.45

0.10

1CTL =

control (n = 45 and 27 litters in parities 1 and 2, respectively), and TRT = treatment regimen (n = 41 and 24 litters in parities 1 and 2, respectively), which provided 70% (restriction) and 115% (overallowance) of the CTL diet in the CP and DE contents. The restriction diet was fed for the first 10 wk of gestation followed by the overallowance diet for the remainder of gestation. 2Maximum

value.

Mammary composition and relative mRNA abundance of selected genes in mammary tissue on d 19 of lactation in first-parity sows are shown in Table 7. There were no differences between treatments for any of the measured variables in terms of mammary composition (P > 0.10), except for parenchymal weight, which tended to be greater in TRT than in CTL sows when values were corrected for BW at slaughter (P < 0.10). There were differences in the relative abundance of mRNA for various genes in mammary parenchyma. Values for CASP3 (P < 0.05), CSN2 (P < 0.01), and PRLR-LR (P < 0.05) were greater and those for WAP (P < 0.01) were lower in parenchyma from TRT than from CTL sows. Evaluation of apoptosis of mammary parenchyma at weaning via immunohistochemistry showed no effect (P > 0.10) on caspase 3 activity (0.22% and 0.21% [maximal SEM = 0.06%] for CTL and TRT sows, respectively) or the TUNEL assay [0.68% and 0.64% (maximal SEM = 0.08%) for CTL and TRT sows, respectively]. Moreover, there were no differences between CTL and TRT sows for the percentage of proliferating mammary cells as measured with the Ki-67 antigen (7.79% and 6.27% [maximal SEM = 0.95%] for CTL and TRT sows, respectively; P > 0.10). Weight, back fat thickness, and feed intakes of sows in second parity are shown in Table 8. The BW of TRT sows was lower than that of CTL sows at mating (P < 0.05) and tended to be lower on d 1 of lactation (P < 0.10), yet there were no differences due to treatment in back fat thickness on any day (P > 0.10). Sow feed intake during lactation also did not differ between treatment groups (P > 0.10). Litter size was similar in both treatment groups (12.23 and

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Table 6. Milk composition on d 17 of lactation1 Groups Item Dry matter, % Fat, % Protein, % Lactose, % Protein quantification (arbitrary units) Casein-beta Whey acidic protein a,bMeans

CTL 18.28 6.99 5.04 5.24 0.97a 3.02a

TRT 17.89 6.66 5.08 5.22

SEM2 0.33 0.32 0.08 0.06

2.52b 1.61b

0.13 0.13

within a row with different superscripts differ (P < 0.01).

1CTL = control (n = 20) and TRT = treatment regimen (n = 20), which pro-

vided 70% (restriction) and 115% (overallowance) of the CTL diet in the CP and DE contents. The restriction diet was fed for the first 10 wk of gestation followed by the overallowance diet for the remainder of gestation. 2Maximum value.

12.75 [maximal SEM = 0.64] for CTL and TRT sows, respectively, P > 0.10), and this was also true for piglet birth weight (1.62 and 1.51 kg [maximal SEM = 0.5 kg] for CTL and TRT sows, respectively; P ≥ 0.10). Statistical analyses done separately on piglet BW for each day showed no effect of treatment (P ≥ 0.10), but the repeated measures in time analyses showed a tendency for piglet BW to be less in TRT than in CTL litters (P < 0.10; Table 5), and there was an effect of day of lactation (P < 0.01) but no treatment × day interaction (P > 0.10). There was a parity effect on BW of piglets (P < 0.001) and on BW gain of piglets from d 1 to 18 of lactation (P < 0.001), with values being greater in parity 2 than parity 1. The postweaning interval to estrus was shorter in TRT than in CTL sows, being 4.25 and 4.81d (maximal SEM = 0.1 d), respectively (P < 0.01). DISCUSSION Few experiments have been performed to determine the effects of nutrition or growth rate of gestating sows on their mammary development. It is known that overfeeding a sow during that period negatively affects mammary development (Head and Williams, 1991). On the other hand, there are indications that diet deprivation followed by overallowance during the growing, finishing, and gestation phases could be beneficial in terms of milk yield and mammary gene expression (Crenshaw et al., 1989). The current results demonstrate that diet deprivation followed by overallowance during the gestation period only (using a dietary regimen similar to that of Crenshaw et al. [1989]) does not improve mammary development at the end of gestation or lactation and does not improve piglet growth rate (i.e., milk yield). It was previously shown that such a dietary regimen in only the growing-finishing period has no beneficial effect on mammary development at the end of gestation (Farmer et al., 2012b), and one would therefore expect that the positive effects observed

Table 7. Mammary gland composition and relative mRNA abundance of selected genes on d 21 of lactation in first-parity sows1 Item Extraparenchymal tissue, g Parenchymal tissue, g Parenchymal tissue/BW on d 21 of lactation, g Dry matter, % Fat,3 % Fat, g Protein,3 % Protein, g DNA,3 mg/g DNA, g total DNA/teat, g Protein/DNA RNA,3 mg/g RNA, g total RNA/teat, g RNA/DNA Mammary relative mRNA abundance4

Groups CTL TRT 1,257.3 1,155.2 2,995.6 3,135.0 16.04e 17.47f 21.0 20.4 36.9 35.2 230.1 227.1 52.7 54.1 330.3 343.8 11.7 12.1 7.34 7.66 1.12 1.15 45.2 45.1 24.3 25.4 15.2 16.2 2.33 2.42 2.08 2.11

CASP3

0.611c

CSN2 GGT1 IGF-1 ODC1 PRLR-LF STAT3 STAT5A STAT5B WAP

0.761a 1.623 0.493 0.463 0.565c 1.175 0.541 0.692 2.704a

0.819d 2.469b 1.569 0.468 0.457 0.706d 1.004 0.454 0.723 1.245b

SEM2 75.0 101.9 0.55 0.3 1.1 11.2 0.9 10.9 0.4 0.26 0.05 0.9 0.7 0.6 0.09 0.05 0.054 0.179 0.110 0.042 0.024 0.040 0.057 0.049 0.062 0.304

a,bMeans

within a row with different superscripts differ (P ≤ 0.01). within a row with different superscripts differ (P < 0.05). e,fMeans within a row with different superscripts tend to differ (P < 0.10). 1CTL = control (n = 14) and TRT = treatment regimen (n = 14), which provided 70% (restriction) and 115% (overallowance) of the CTL diet in the CP and DE contents. The restriction diet was fed for the first 10 wk of gestation followed by the overallowance diet for the remainder of gestation. 2Maximum value. 3Expressed on a dry matter basis. 4Relative mRNA abundances. Values correspond to the relative abundance of studied genes’ mRNA. CASP3, caspase 3; CSN2, casein beta; GGT1, gamma-glutamyltransferase 1; IGF-1, insulin-like growth factor 1; ODC1, ornithine decarboxylase 1; PRLR-LF, long form of the prolactin receptor; STAT3, STAT5A, and STAT5B, signal transducers and activators of transcription 3, 5A, and 5B; WAP, whey acidic protein. c,dMeans

by Crenshaw et al. (1989) were most likely due to a gestation effect. Yet the current results do not support that theory. However, there could be other reasons for these unexpected findings. First, there were differences in diet composition between the 2 studies. In the study by Crenshaw et al. (1989), sunflower hulls were used as a fiber source (Crenshaw, 1990), whereas in the current study, soybean hulls, wheat soft, and wheat middlings were the sources of fiber. Second, feed intake per day varied between

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Gestation feeding and mammary development in gilts

Table 8. Weight, back fat thickness, and feed intake in second-parity sows1 Groups Item BW, kg Mating d 108 of gestation Gain, mating to d 108 d 1 of lactation d 17 of lactation Loss from d 1 to 17 Back fat, mm Mating d 108 of gestation Gain, d 70 to 108 d 1 of lactation d 17 of lactation Loss from d 1 to 17 Average daily feed intake, kg d 1 to 17 of lactation

CTL

TRT

SEM2

179.8c 249.0 69.2 228.1e 212.4 15.7

171.0d 242.9 71.9 220.7f 205.4 15.3

2.7 2.7 2.0 2.8 3.2 1.8

134.5 16.5 3.0 14.9 13.0 1.9

13.6 17.3 3.7 15.9 14.0 1.9

0.6 0.6 0.4 0.5 0.5 0.3

5.92

5.57

0.27

c,dMeans

within a row with different superscripts differ (P < 0.05). within a row with different superscripts tend to differ (P < 0.10). 1CTL = control (n = 27) and TRT = treatment regimen (n = 24), which provided 70% (restriction) and 115% (overallowance) of the CTL diet in the CP and DE contents. The restriction diet was fed for the first 10 wk of gestation followed by the overallowance diet for the remainder of gestation. 2Maximum value. e,fMeans

the trials. Crenshaw (1990) fed 1.81 kg/d in gestation, whereas in the current study, 2.27 kg/d were provided. However, the relative differences between the TRT and CTL groups in terms of dietary protein and DE contents were similar. Third, even though growth rate was greater for TRT than CTL sows during the feed overallowance phase (d 70 onward) in the current study, growth rate over the whole gestation period was reduced by 11 kg in TRT sows (compared with a 5.9-kg difference in the trial by Crenshaw et al. [1989]), so that their BW and back fat thickness at slaughter were also reduced (which was not the case in the trial by Crenshaw et al. [1989]). Therefore, when beneficial effects of a compensatory regimen during gestation were observed in rodents, BW was not reduced at the end of gestation in treated animals (Kim and Park, 2004). One wonders whether the restriction imposed in the current study was too severe or whether it should have been done over a shorter period of time to exert beneficial effects. Because the percentage differences in DE and protein contents between the restriction and the overallowance diet, relative to the CTL diet, were similar in the current study and that of Crenshaw et al. (1989), the most likely explanation for the discrepancy in growth rate is the different sources of fiber, which may have affected nutrient use and digestibility (Matte et al., 1994). It is known that feed restriction (i.e., reduced growth) during the growing-finishing period in swine negatively

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affects mammary development at puberty (Farmer et al., 2004; Sorensen et al., 2006), and the current results indicate that this is also the case in gestation. Such an effect of plane of nutrition in gestation on mammary development was also demonstrated in ewes, where feeding 60% of requirements from d 50 of gestation onward reduced mammary gland weight and colostrum yield 24 h postpartum (Swanson et al., 2008). A similar restriction starting on d 50 of gestation reduced colostrum and milk yield in primiparous ewes (Meyer et al., 2011). The effect of body condition per se on mammogenesis has yet to be determined. Overly fat sows (36 vs. 24 mm back fat) have a stunted mammary development at the end of gestation (Head and Williams, 1991), and the current findings would indicate that sows that are too thin (16.1 mm for TRT vs. 17.5 mm for CTL) also have reduced mammary development in late gestation, as shown by a reduction in parenchymal tissue mass. Interestingly, the composition of parenchymal tissue was not altered by feeding regimen. The extent of the difference between CTL and TRT sows in terms of parenchymal tissue mass was less when data were corrected for BW (18%) than when they were not corrected (25%), yet they still differed, indicating that the treatment effect on mammary parenchyma cannot be accounted for by changes in BW alone. These differences in mammary composition between TRT and CTL sows were not present at the end of lactation, indicating that piglets were able to compensate for this negative effect, possibly via suckling intensity and udder stimulation (Kim et al., 2000). Indeed, piglets from TRT and CTL sows had similar BW throughout lactation. To the best of our knowledge, this is the first demonstration of such a catching-up effect in mammary development during lactation, and it would be interesting to know whether this would also be the case in multiparous sows where, in contrast to primiparous sows, there is no further increase in cell number during lactation (Manjarin et al., 2011). Another possibility for the different treatment effects on mammary development at the end of gestation and lactation could be the alterations in relative abundance of various genes between TRT and CTL sows in parenchymal tissue at these times. For instance, expression level for IGF-1 was lower in TRT than CTL sows in gestation but was not altered in lactation. Knowing the importance of IGF-1 for mammary development in rodents (Kleinberg and Barcellos-Hoff, 2011), this could have partly accounted for the reduced parenchymal tissue. The enzyme ODC1 is highly regulated and catalyzes the first step in the biosynthesis of polyamines, which play key roles in cell proliferation and differentiation (Pegg and McCann, 1982; Cohen, 1998). Its transcription is regulated by many factors, including hormones and growth factors, and its activity increases in mammary epithelial cells of pregnant and early lactating mice (Pegg, 2006).

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In mammary tissues collected in early lactation, the ODC1 mRNA abundance was found to be greater in rats fed a compensatory nutrition regimen compared with rats receiving a control diet (Moon and Park, 1999; Kim and Park, 2004). In the current study, there was no difference between TRT and CTL sows for ODC1 mRNA abundance in early lactation, whereas ODC1 mRNA level was lower in TRT than in CTL sows in late gestation. Discrepancies may be explained, at least in part, by species differences or by the different sources of fiber used. Indeed, Janicke et al. (2011) recently reported that the ODC1 gene expression was downregulated when Caco-2 colon cancer cells were treated with para-coumaric acid, a dietary fiber phenolic compound. Expression of the CSN2 gene was increased in mammary tissue from TRT compared with CTL sows at the end of both gestation and lactation, and CSN2 protein in milk corresponded with CSN2 mRNA levels during lactation. In heifers, expression of CSN2 in mammary tissue in late gestation was associated with increased mammary development (Ford and Park, 2001). However, the current findings preclude such a relationship between CSN2 expression and mammary development in swine. Relative mRNA abundance for PRLR-LF was greater in TRT than in CTL sows in lactation but was similar in gestation, and that of STAT5B (a mediator of prolactin action) was less for TRT than for CTL sows in late gestation and similar in late lactation. This last finding indicates a potential involvement of STAT5B in mammogenesis in late pregnant gilts and supports our previous findings of a positive correlation (r = 0.84) between parenchymal weight and STAT5B, but not STAT5A, mRNA levels in Large White gilts (Palin et al., 2002). The increased mammary expression of the CASP3 gene in TRT vs. CTL sows at the end of lactation should denote a greater rate of cell death (Kim and Park, 2004), yet this was not associated with less mammary development in the current study. The protein WAP is a known downstream target of STAT5 transcriptional regulators (Li and Rosen, 1995) and plays an important role in regulating mammary epithelial cell proliferation (Nukumi et al., 2007). However, when using WAP knockout mice, Triplett et al. (2005) observed that WAP was necessary for adequate development of the young in late lactation but not for differentiation of mammary parenchymal cells. In the current study, WAP mRNA abundance was less for TRT than for CTL sows in late gestation and similar for both groups in late lactation, and WAP protein abundance in milk was also less in TRT than in CTL sows. These findings may indicate a relationship between CSN2 expression and mammary development in sows, as lower WAP gene and protein expression is observed in animals having lower parenchymal tissue weights. Changes in circulating metabolites were as expected for underfed and overfed animals. The greater concen-

trations of FFA at the end of the restricted period and lower concentrations at the end of the overallowance period likely reflect the increased and decreased use of energy reserves during those respective periods (Barb et al., 1997). Lower concentrations of IGF-1 at the end of the restriction period concur with the decreased growth rate and are indicative of a negative energy balance. A decrease in IGF-1 was previously observed when a similar diet deprivation was imposed on prepubertal gilts (Farmer et al., 2012a). The absence of alterations in circulating concentrations of IGF-1 and metabolites between treatments during lactation, coupled with the similar sow feed intakes, are in agreement with the lack of treatment effect on milk composition. In conclusion, feed deprivation and subsequent overallowance in gestation had unfavorable effects in terms of lower sow BW and back fat gains during gestation and reduced mammary parenchyma and mammary expression of specific genes (such as IGF-1, ODC1, STAT5B, and WAP) at the end of gestation, but piglet growth rate over 2 parities was not affected. However, it still needs to be determined whether compensatory gain (i.e., restricted growth followed by overcompensation in growth) during the phase of rapid mammary accretion in late gestation could have a beneficial impact on mammary development and subsequent milk yield in swine. Literature Cited Agriculture and Agri-Food Canada. 1993. Recommended code of practice for the care and handling of farm animals—Pigs. Publ. No. 1898E. Agric. Agri-Food Can., Ottawa, ON. Andersen, C. L., J. L. Jensen, and T. F. Orntoft. 2004. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64:5245–5250. AOAC. 2005. Official methods of analysis international. 18th ed. Assoc. Off. Anal. Chem, Arlington, VA. Applied Biosystems. 1997. ABI PRISM 7700 sequence detection system. User Bull. No. 2. Appl. Biosyst., Foster City, CA. Barb, C. R., R. R. Kraeling, G. B. Rampacek, and C. R. Dove. 1997. Metabolic changes during the transition from the fed to the acute feed-deprived state in prepubertal and mature gilts. J. Anim. Sci. 75:781–789. Cohen, S. S. 1998. A guide to polyamines. Oxford Univ. Press, New York. p. 231–259. Crenshaw, J. D. 1990. Feeding gilts to enhance lactational performance. In: North Dakota State University Swine Research Report. Agric. Exp. Stn. Ext. Serv., Fargo, ND. p. 12–23. Crenshaw, J. D., C. S. Park, P. M. Swantek, W. L. Keller, and R. C. Zimprich. 1989. Lactation response of gilts to a phased feeding regimen designed to induce compensatory growth. J. Anim. Sci. 67(Suppl. 2):107–108. (Abstr.) Farmer, C., M. F. Palin, and Y. Martel-Kennes. 2012a. Impact of diet deprivation and subsequent over-allowance during prepuberty. Part 1. Effects on growth performance, metabolite status, and mammary gland development in gilts. J. Anim. Sci. 90:863–871.

Downloaded from www.journalofanimalscience.org at Universite Laval on July 13, 2014

Gestation feeding and mammary development in gilts Farmer, C., M. F. Palin, and Y. Martel-Kennes. 2012b. Impact of diet deprivation and subsequent over-allowance during prepuberty. Part 2. Effects on mammary gland development and lactation performance of sows. J. Anim. Sci. 90:872–880. Farmer, C., D. Petitclerc, M. T. Sorensen, M. Vignola, and J. Y. Dourmad. 2004. Impacts of dietary protein level and feed restriction during prepuberty on mammogenesis in gilts. J. Anim. Sci. 82:2343–2351. Ford, J. A., Jr., and C. S. Park. 2001. Nutritionally directed compensatory growth enhances heifer development and lactation potential. J. Dairy Sci. 84:1669–1678. Harrell, R. J., M. J. Thomas, and R. D. Boyd. 1993. Limitations of sow milk yield on baby pig growth. In: Proc. Cornell Nutr. Conf., Rochester, NY. p. 156. Head, R. H., and I. H. Williams. 1991. Mammogenesis is influenced by pregnancy nutrition. In: Manipulating pig production III. Australas. Pig Sci. Assoc., Werribee, Victoria, Australia. p. 33. Huntington, G. B. 1984. Net absorption of glucose and nitrogenous compounds by lactating Holstein cows. J. Dairy Sci. 67:1919–1927. Janicke, B., C. Hegardt, M. Krogh, G. Onning, B. Akesson, H. M. Cirenajwis, and S. M. Oredsson. 2011. The antiproliferative effect of dietary fiber phenolic compounds ferulic acid and p-coumaric acid on the cell cycle of Caco-2 cells. Nutr. Cancer 63:611–622. Kim, H. H., and C. S. Park. 2004. A compensatory nutrition regimen during gestation stimulates mammary development and lactation potential in rats. J. Nutr. 134:756–761. Kim, S. H., Y. S. Moon, W. L. Keller, and C. S. Park. 1998. Compensatory nutrition-directed mammary cell proliferation and lactation in rats. Br. J. Nutr. 79:177–183. Kim, S. W., W. L. Hurley, I. K. Han, and R. A. Easter. 2000. Growth of nursing pigs related to the characteristics of nursed mammary glands. J. Anim. Sci. 78:1313–1318. Kleinberg, D. L., and M. H. Barcellos-Hoff. 2011. The pivotal role of insulin-like growth factor I in normal mammary development. Endocrinol. Metab. Clin. North Am. 40:461–471. Labarca, C., and K. Paigen. 1980. A simple, rapid, and sensitive DNA assay procedure. Anal. Biochem. 102:344–352. Labrecque, B., D. Beaudry, M. Mayhue, C. Hallé, V. Bordignon, B. D. Murphy, and M. F. Palin. 2009. Molecular characterization and expression analysis of the porcine paraoxonase 3 (PON3) gene. Gene 443:110–120. Li, S., and J. M. Rosen. 1995. Nuclear factor I and mammary gland factor (STAT5) play a critical role in regulating rat whey acidic protein gene expression in transgenic mice. Mol. Cell. Biol. 15:2063–2070. Lyvers-Peffer, P. A., and D. W. Rozeboom. 2001. The effects of a growth-altering pre-pubertal feeding regimen on mammary development and parity-one lactation potential in swine. Livest. Prod. Sci. 70:167–173. Manjarin, R., N. L. Trottier, P. S. Weber, J. S. Liesman, N. P. Taylor, and J. P. Steibel. 2011. A simple analytical and experimental procedure for selection of reference genes for reverse-transcription quantitative PCR normalization data. J. Dairy Sci. 94:4950–4961.

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Matte, J. J., S. Robert, C. L. Girard, C. Farmer, and G.-P. Martineau. 1994. Effect of bulky diets based on wheat bran or oat hulls on reproductive performance of sows during their first two parities. J. Anim. Sci. 72:1754–1760. Meyer, A. M., J. J. Reed, T. L. Neville, J. F. Thorson, K. R. MaddockCarlin, J. B. Taylor, L. P. Reynolds, D. A. Redmer, J. S. Luther, C. J. Hammer, K. A. Vonnahme, and J. S. Caton. 2011. Nutritional plane and selenium supply during gestation affect yield and nutrient composition of colostrum and milk in primiparous ewes. J. Anim. Sci. 89:1627–1639. Moon, Y. S., and C. S. Park. 1999. Nutritionally-directed compensatory growth enhances mammary development and lactation potential in rats. J. Nutr. 129:1156–1160. Moon, Y. S., and C. S. Park. 2002. Effects of controlled compensatory growth on mammary gland development and lactation in rats. Asian-Australas. J. Anim. Sci. 15:1364–1370. Nukumi, N., T. Iwamori, K. Kano, K. Naito, and H. Tojo. 2007. Whey acidic protein (WAP) regulates the proliferation of mammary epithelial cells by preventing serine protease from degrading laminin. J. Cell. Physiol. 213:793–800. Palin, M. F., D. Beaudry, C. Roberge, and C. Farmer. 2002. Expression levels of STAT5A and STAT5B in mammary parenchymal tissu from Upton-Meishan and Large White gilts. Can. J.Anim. Sci. 82:507-518. Pegg, A. E. 2006. Regulation of ornithine decarboxylase. J. Biol. Chem. 281:14529–14532. Pegg, A. E., and P. P. McCann. 1982. Polyamine metabolism and function. Am. J. Physiol. Cell Physiol. 243:C212–C221. Plante, P.-A., J.-P. Laforest, and C. Farmer. 2011. Effect of supplementing the diet of lactating sows with NuPro® on their performances and that of their piglets. Can. J. Anim. Sci. 91:295–300. Robert, S., A. M. B. de Passillé, N. St-Pierre, P. Dubreuil, G. Pelletier, D. Petitclerc, and P. Brazeau. 1989. Effect of the stress of injection on the serum concentrations of cortisol, prolactin, and growth hormone in gilts and lactating sows. Can. J. Anim. Sci. 69:663–672. Sorensen, M. T., C. Farmer, M. Vestergaard, S. Purup, and K. Sejrsen. 2006. Mammary development in prepubertal gilts fed restrictively or ad libitum in two sub-periods between weaning and puberty. Livest. Sci. 99:249–255. Sorensen, M. T., K. Sejrsen, and S. Purup. 2002. Mammary gland development in gilts. Livest. Prod. Sci. 75:143–148. Swanson, T. J., C. J. Hammer, J. S. Luther, D. B. Carslon, J. B. Taylor, D. A. Redmer, T. L. Neville, J. J. Reed, L. P. Reynolds, J. S. Caton, and K. A. Vonnahme. 2008. Effects of gestational plane of nutrition and selenium supplementation on mammary development and colostrum quality in pregnant ewe lambs. J. Anim. Sci. 86:2415–2423. Triplett, A. A., K. Sakamoto, L. A. Matulka, L. Shen, G. H. Smith, and K. U. Wagner. 2005. Expression of the whey acidic protein (Wap) is necessary for adequate nourishment of the offspring but not for functional differentiation of mammary epithelial cells. Genesis 43:1–11. Volkin, E., and W. E. Cohn. 1954. Estimation of nucleic acids. Methods Biochem. Anal. 1:287–305.

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Impact of diet deprivation and subsequent overallowance during gestation on mammary gland development and lactation performance.

The impacts of diet deprivation and subsequent overallowance during gestation on mammary gene expression and development and lactation performance wer...
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