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Effects of suckling intensity on milk yield and piglet growth from lactation-enhanced gilts¹

K. M. Marshall^*, W. L. Hurley^*,2, R. D. Shanks^* and M. B. Wheeler^*,,3

^* University of Illinois, Department of Animal Sciences, and and Beckman Institute for Advanced Science and Technology, Urbana, IL 61801

	Abstract

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The effects of suckling intensity on milk yield and piglet growth were determined when lactation capacity of the sow was enhanced through overexpression of a mammary-specific transgene, bovine -lactalbumin. Lactational response to increased suckling stimulation was determined by fostering litters of the same age (d 1) or 7 d older (d 7) than the day of lactation to sows nontransgenic (control) or transgenic (TG) for bovine -lactalbumin. Twenty first-parity gilts were allocated to 4 treatments dependent on gilt genotype and age of litter fostered (control d 1, control d 7, TG d 1, and TG d 7). Litters were standardized to 10 piglets within 24 h postpartum, and nonbirth piglets were fostered to gilts with an equal litter BW within age groups at 36 h postpartum. Milk yield was determined by the weigh-suckle-weigh method on d 6, 9, 12, 15, and 18 of lactation. Mean daily milk yield was greater (P = 0.031) for TG gilts compared with control gilts and tended to be greater (P = 0.056) for all gilts with d-7 piglets compared with those with d-1 piglets. Daily milk yield of TG d 7 gilts increased rapidly to peak at d 9 and was greater than milk yield of all control gilts at d 9 (P < 0.01), 12 (P < 0.02), and 15 (P < 0.02). Mean daily milk yield of TG d 7 gilts was 2.1 kg greater (P = 0.002) than for control d 7 gilts and 2.0 kg greater (P = 0.004) than for TG d 1 gilts. Daily milk yield of control d 1 gilts was not different from that of TG d 1 gilts (P = 0.49) or control d 7 gilts (P = 0.63). Piglet BW gain between d 3 and 6 was greater (P < 0.01) in the TG d 7 group than for all other groups and was greater (P < 0.05) than the control groups between d 6 and 9. No difference was found when comparing accumulated BW gain of the piglets between the day of age at foster (d 1 vs. 7; P = 0.606) or between the control d 1 and control d 7 groups (P = 0.759). Accumulated BW gain of piglets suckling TG d 7 gilts from d 3 through 9 was greater (P < 0.02) than that of the other groups and continued to be greater (P < 0.05) than that of either of the control groups through d 15. However, by d 15, accumulated BW gain of piglets suckling TG d 1 gilts was no longer different (P = 0.40) from that of the TG d 7 group and was greater (P < 0.05) than that of the control d 1 group. The enhanced lactation potential of these TG gilts synergized with suckling intensity to stimulate increased milk production during early lactation, resulting in increased piglet growth.

Key Words: -lactalbumin • milk yield • piglet growth • suckling intensity • swine • transgenic animal

	INTRODUCTION

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Milk production by the sow is one of the most important factors limiting neonate piglet growth (Boyd and Kensinger, 1998). Milk removal is critical in the regulation of milk secretion. In swine, milk yield is affected by the level of suckling intensity, which encompasses several sow-litter interactions, including suckling frequency, litter size, and age and size of piglets (reviewed by King, 2000). Increased suckling intensity would be expected to cause an increase in total mammary cell numbers (Wilde and Peaker, 1990). Indeed, mammary gland DNA doubles during lactation in gilts (Kim et al., 1999a), and the extent of postpartum growth is affected by litter size (Kim et al., 1999b). In addition, differentiation state of mammary cells contributes to the early increase in milk yield in ruminants (Knight and Peaker, 1984; Wilde et al., 1987). Less certain is the role of mammary cell differentiation state in regulation of milk production by the sow.

Alteration of the normal metabolism of the mammary gland of the sow by transgenic (TG) overexpression of -lactalbumin (-LA) results in increased milk yield and increased piglet BW gain (Noble et al., 2002). The bovine -LA transgene product is expressed at elevated concentrations during the initial days of lactation, compared with the porcine gene product (Bleck et al., 1998), and colostrum and milk composition are altered in early lactation (Noble et al., 2002). This early enhancement of mammary differentiation state in the -LA TG sows also may result in greater responsiveness to suckling intensity. This study determined the responsiveness of control and TG sows to different levels of suckling intensity, as defined by age of piglets suckling in early lactation. Transgenic sows exposed to increased suckling intensity in early lactation produced more milk than those subjected to less suckling intensity.

	MATERIALS AND METHODS

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Animals

The animal use and care protocol was approved by the Institutional Animal Care and Use Committee of the University of Illinois. Yorkshire gilts, heterozygous for the bovine -LA transgene, were produced as described previously (Bleck et al., 1998). Lactation performance of first-parity bovine -LA TG gilts has been previously reported (Noble et al., 2002). As female descendents from the founder boar attained puberty, non-transgenic control and TG gilts were bred to a Yorkshire boar by AI. On d 109 of pregnancy, gilts were moved into the farrowing house and monitored for signs of parturition. Gilts and their newborn piglets were monitored during farrowing to assure a safe delivery and that successful nursing occurred. Litter size initially was established within 24 h of parturition at 10 piglets per gilt.

Between 30 and 42 h postpartum, birth-litters were removed from the gilts and replaced with litters composed of 10 nonbirth piglets in an equal sex ratio and balanced by BW within age. Piglets used in replacement litters were born to control gilts or nontransgenic sows of comparable genetics to that of the control gilts. In no case did a piglet suckle its own mother after crossfostering. Litters consisting of piglets that were the same age as the day of lactation for the sow were identified as d 1 litters, and litters consisting of piglets approximately 7 d older than the day of lactation of the sow were identified as d 7 litters. Therefore, treatment groups were identified as control d 1 (n = 6 gilts with litters), control d 7 (n = 5), TG d 1 (n = 5), and TG d 7 (n = 4). Mean BW of piglets at fostering (d 2) was 1,782 ± 95 g for the control d 1 group, 3,338 ± 116 g for the control d 7 group, 1,746 ± 104 g for the TG d 1 group, and 3,363 ± 116 g for the TG d 7 group. The sow’s milk was the only source of nutrition for the piglets during the lactation period. Piglets did not have access to the feed of the sow. There was no piglet loss after crossfostering.

Milk Production Analysis

Milk production by gilts was measured on d 6, 9, 12, 15, and 18 of lactation by a modification of the weigh-suckle-weigh (WSW) method of Speer and Cox (1984), as described previously (Noble et al., 2002). Briefly, litters were separated from their dams for 1 h. Piglets were placed in a pen under a heat lamp during the separation. Litters then were weighed to obtain a pre-suckling BW, returned to their mothers, allowed to suckle until the end of vigorous synchronized suckling by the litter, and then immediately collected and weighed after suckling to obtain a postsuckling BW. This procedure was repeated hourly until a minimum of 3 consistent measurements of hourly milk yield were obtained. Hourly milk yields were a measurement of BW gain due to litter milk intake determined from the difference between pre- and postsuckling litter BW. Mean hourly milk yield multiplied by 24 was used for an estimate of daily milk yield. Suckling frequency was not controlled on the other days of lactation.

Litter Performance Analysis

To examine differences in TG- and control-reared litters, birth weight, weaning weight, litter weight gain after birth, and ADG were recorded. In addition, individual piglet BW initially was recorded daily from day of foster (d 2) until d 6 and subsequently recorded every third day until d 18. Litter weights were the sum of all piglet BW within each litter. Multiple growth periods for piglets were analyzed from d 3 to 6, 6 to 9, 9 to 12, 12 to 15, and 15 to 18. Accumulated BW gains were analyzed for periods from d 3 to d 6, 9, 12, 15, and 18, respectively. Growth data for piglets suckling gilts were analyzed by mean piglet growth per each gilt suckled, with each gilt then being a replicate within treatment.

Statistical Analysis

Milk production for each lactating gilt was analyzed on WSW days for individual outlier data points. Outlier data points were excluded if they were greater than 3 SD from the mean of the remaining data points. Data excluding outliers were then incorporated into further treatment analysis. Dependent variables included 1 of the 4 following measurements: mean gilt milk yield per treatment day (kg/d), overall mean gilt milk yield for the experimental period (kg/d), 3-d mean piglet growth measurements (g/3 d), or cumulative mean piglet growth measurements (d 3 through 18; g/15 d). Independent variables included treatment (genotype x day of foster), sow, and day of WSW (dWSW).

The GLM for gilt mean milk yield was: y_ijk = µ + (ß)_ij + e_ijk, where µ was the general mean, (ß)_ij was a joint treatment effect partitioned into _i for the genotype effect of the TG or control gilt, ß_j for the age effect of the 1 or 7 d of foster, and the interaction between genotype and day of foster, and e_ijk was the normally distributed random experimental error of the kth gilt within the treatment. Partitioning occurred via contrasts for each main effect (gilt genotype and litter age), as well as the interaction between genotype and litter age. In further analysis, a split-plot model was performed to provide additional information on the repeated measurement of dWSW. The split-plot model was y_ijk = µ + (ß)_ij + s_ijk + d_l + (ßd)_ijl + e_ijkl, where µ was the general mean, (ß)_ij was a joint effect partitioned into _i for the genotype effect of the TG or control gilt, ß_j for the age effect of the 1 or 7 d of foster, and the interaction of genotype x day of foster, s_ijk was the gilt effect and main plot error, d_l was the dWSW, (ßd)_ijl was the interaction of treatment x dWSW, and e_ijkl was the normally distributed random subplot experimental error. The GLM procedure of SAS (SAS Inst. Inc., Cary, NC) was used to estimate significances, least squares means, contrasts, and SE.

	RESULTS

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Milk Yield

Daily milk yield for the overall period between d 6 and 18 was approximately 16% greater (P = 0.031) for the TG gilts compared with control gilts (Table 1). In addition, average daily milk yield for the entire lactation tended (P = 0.056) to be greater for gilts nursing piglets fostered at d 7 of age compared with those nursing piglets fostered at d 1 of age. Daily milk yield of the TG d 7 gilts increased rapidly to a peak at about d 9, and then declined slowly (Table 1). Daily milk yield of TG d 7 gilts was consistently greater (P < 0.02) than milk yield of control gilts of either day of foster group between d 9 and 15 and continued to be greater (P = 0.009) than that of the control d 1 gilts at d 18. Mean daily milk yield of TG d 7 gilts for the period between d 6 and 18 was 30% greater (2.1 kg; P = 0.022) than for the control d 7 gilts and 28% greater (2.0 kg; P = 0.004) than for the TG d 1 gilts. Daily milk yields of TG d 1 gilts were not different (P = 0.49) from those of the control d 1 gilts. Daily milk yield of control d 7 gilts was not different (P = 0.63) from that of control d 1 gilts, except at d 18, when control d 7 gilts tended to have greater (P = 0.08) milk yields than the control d 1 gilts.

Piglet BW gain was determined for 3-d intervals beginning at d 3 of lactation (Table 2). This allowed for the initial period of cross-fostering (within 30 to 42 h postpartum) plus an additional day for fostered litters to establish teat order and synchronized sucklings. Overall, 3-d BW gain was greater for piglets suckling TG gilts than control gilts (P = 0.012; Table 2). On the other hand, overall 3-d BW gain was not different for d 1 piglets vs. d 7 piglets (P = 0.559). Differences in 3-d BW gain were apparent early in lactation, between d 3 and 6 (P = 0.001), and d 6 and 9 (P = 0.035). Piglets suckling lactation-enhanced gilts of the TG d 7 group had greater (P 0.005) 3-d BW gains than all other groups for the period of d 3 to 6, and greater gains than the control d 1 (P = 0.006) and control d 7 (P = 0.025) groups for the period of d 6 to 9 (Table 2).

	DISCUSSION

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First parity milk production for this line of bovine LA TG gilts has been reported previously (Noble et al., 2002). These gilts produce bovine -LA in their milk during lactation. This additional -LA expression results in a mammary gland that produces milk at a greater level than produced by control gilts, at least during early lactation. Expression of bovine -LA in the mammary gland results in synthesis and secretion of lactose (Bleck et al., 1998; Noble et al., 2002). Expression of -LA and synthesis of lactose are indicators of the potential response of the tissue to a range of factors that regulate lactation in swine and that may enhance the lactation capacity of the mammary gland.

Suckling intensity is a major determinant of milk production and mammary development during lactation in swine (King, 2000; Hurley, 2001). Suckling intensity encompasses several sow-litter interactions, including suckling frequency, litter size, and age and size of piglets, each of which has an impact on the removal of milk from the mammary gland. Decreasing suckling frequency by increasing intersuckling interval results in increased milk intake per suckling but decreased overall daily milk production by the sow (Spinka et al., 1997). On the other hand, increasing suckling frequency results in increased milk yield, as well as increased mammary parenchymal tissue (Auldist et al., 1995). A sow is capable of supporting 2 litters when suckling frequency is controlled (Sauber et al., 1994). Litter size also is a significant determinant of total milk production by a lactating sow (King, 2000). Milk intake by each piglet, however, is reduced as litter size increases. Increasing litter size results in similar responses in mammary growth in lactating gilts (Kim et al., 1999b).

Sow milk yield is affected by the demand for milk by suckling piglets. Heavier piglets are able to stimulate a greater milk flow from sows (Van der Steen and de Groot, 1992; King et al., 1997) and may empty their glands more completely (Hartman et al., 1962) than lighter piglets. Larger piglets may massage the teat more vigorously before milk ejection, thus achieving a greater blood flow to the teat and thereby bring more of the limited supply of oxytocin to the mammary gland (Fraser, 1984). The secretion of prolactin also may be influenced by increased massage of the udder (Algers, 1993; King, 2000). Blood prolactin in sows is increased during suckling (Plaut et al., 1989). Overall, increased milk yield in response to heavier piglets is associated with increased production per gland (Auldist et al., 2000).

The current study took advantage of the relationship between piglet age and intensity of suckling, as well as minimizing the extent of downregulation of milk synthesis due to incomplete milk removal in the early stages of lactation. This model is based on replacing newborn piglets with older piglets that remove more milk during each suckling bout. The resultant milk yield should be closer to the genetic potential of the sow for milk production (Mackenzie and Revell, 1998). Using a similar model, King et al. (1997) found an increase in milk yield of 20% or more during the initial week of lactation when fostering 2-wk-old piglets onto newly farrowed sows, although milk yield was not different from controls by midlactation. The general lack of significant enhancement of milk production in the current study by nontransgenic gilts nursing the 7-d old piglets, compared with nontransgenic gilts nursing piglets age-matched to the day of lactation, suggests that the increase in suckling intensity elicited by the 7-d-old piglets may not be as great as that if 14-d-old piglets are cross-fostered. A lack of effect of piglet age also may have been the result of the limited numbers of gilts in the current study. On the other hand, the level of suckling intensity provided by the 7-d-old piglets resulted in a rapid and early increase in milk yield in the TG gilts. The rate of increase in milk yield between d 6 and 9 of lactation by TG gilts nursing 7-d-old piglets at the beginning of the study was about 0.9 kg/d, compared with about 0.5 kg/d for the nontransgenic gilts nursing the 7-d-old piglets during that same period.

Previous characterization of this line of bovine -LA TG swine, including 20 pairs of full-sibling non-transgenic and heterozygous TG gilts, indicated that milk yield is enhanced under a normal suckling regimen only in the first third of lactation (Noble et al., 2002). In the current study, the limited number of gilts per group (4 to 6 gilts per group) does not provide sufficient statistical power to determine the difference between milk production of the control and TG gilts nursing the 1-d-old piglets, but clearly is sufficient to determine the effect of the increased suckling intensity on milk production by the TG gilts. Results of the current study demonstrate an increased rate of growth during later lactation by 1-d-old piglets suckling TG gilts compared with those suckling control gilts. Accumulated BW gain after birth was about 11% greater at d 18 of lactation for piglets suckling TG gilts vs. control gilts in the previous study of Noble et al. (2002), and in the current study accumulated gain between d 3 and 18 was about 14% greater for piglets suckling TG vs. control gilts.

Differences in milk composition between TG and control gilts are found only in the early stages of lactation (Noble et al., 2002). In the current study, all piglets from unrelated sows were cross-fostered onto the experimental gilts at d 2 and after the stage of colostrum secretion, precluding any potential confounding effect of colostrum consumption on subsequent piglet growth. By d 3 of lactation, the composition of milk from TG gilts is not different from control gilts; however, the increased milk production results in greater intake of solids by the piglets (Noble et al., 2002). Several lines of evidence indicate that the nutrients ingested by the newborn animal early in lactation will affect later growth and development (Davis et al., 1989, 1998; Reeds et al., 2000; Hales and Ozanne, 2003). Indeed, low milk production by the sow has long range effects resulting in reduced growth rates before weaning and suboptimal growth postweaning through the grower and finisher stages (Hartmann et al., 1984).

The current study demonstrates a synergy between suckling intensity and lactation capacity of the mammary gland in swine. This study highlights the need to gain a better understanding of the role of the differentiation state of the mammary gland during early lactation in regulation of milk production and of how that level of differentiation is affected by suckling and milk removal by the piglet.

	Footnotes

 
¹ This material is based on work partially supported by the Illinois Council for Food and Agricultural Research (C-FAR) Sentinel Program, the USDA Cooperative State Research, Education and Extension Service Regional Research Project W-171, and the Illinois Agric. Exp. Stn. as part of Hatch Project 538-327. The authors would like to thank J. Cook, S. Lane, and M. Monaco who contributed technical assistance to the work described herein.

³ Reprints: mbwheele{at}uiuc.edu, 1027 West Gregory Drive, Urbana, IL 61801.

² Corresponding author: wlhurley{at}uiuc.edu

Received for publication December 26, 2005. Accepted for publication May 2, 2006.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 


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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Marshall, K. M. Articles by Wheeler, M. B. Search for Related Content PubMed PubMed Citation Articles by Marshall, K. M. Articles by Wheeler, M. B.