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Relationships between piglet growth rate and mammary gland
size of the sow
a b a ,
*
O.L. Nielsen , A.R. Pedersen , M.T. Sørensen
a
Department of Animal Nutrition and Physiology, Danish Institute of Agricultural Sciences, Foulum Research Centre, P.O. Box 50, DK-8830 Tjele, Denmark
b
Department of Agricultural Systems, Danish Institute of Agricultural Sciences, Foulum Research Centre, P.O. Box 50, DK-8830 Tjele, Denmark
Received 22 February 1999; received in revised form 10 December 1999; accepted 30 March 2000
Abstract
An experiment was conducted to study whether piglet growth rate is related to mammary gland size. It involved three primiparous sows and four multiparous sows that were fed ad libitum during the lactation period. The piglets received no creep feed. The weight and teat order of the piglets were recorded. The sows were slaughtered after approximately 4 weeks of lactation (25–28 days). The amounts of mammary tissue and mammary DNA were larger in multiparous than in primiparous sows, and the concentrations and amounts of mammary RNA as well as mammary RNA / DNA ratios were highest in the front glands, intermediate in the middle and lowest in the rear glands. Average daily gain of the piglets was of the same magnitude regardless of gland position in the primiparous sows. In the multiparous sows, the piglets suckling the front teats had the highest gain while those suckling the middle teats had intermediate gain and those suckling the rear teats had the lowest gain. Average daily gain of the piglets in the lactation period was positively correlated to the amount of mammary tissue (0.35), mammary DNA (0.41) and mammary RNA (0.31), while correlations to mammary RNA concentration (0.28) and RNA / DNA ratio (0.22) did not reach significance. There were no significant correlations between piglet start weight and any of these mammary gland compositional traits. 2001 Elsevier Science B.V. All rights reserved.
Keywords: Pig reproduction; Piglet growth rate; Milk yield; Mammary gland size
1. Introduction Until weaning at the age of 4 weeks, sow milk is the main energy source for the piglets. Sørensen et In pig production it is important that the piglets al. (1998) reported that in the third and fourth week are big and uniform at weaning. To ensure this, the of lactation, piglets consumed creep feed, corre-sow must have a high and uniform milk yield in all sponding to only approximately 2–3% of the milk productive mammary glands. energy consumed in the same period.
The number of milk producing cells and the activity of these cells appear to determine milk yield *Corresponding author. Tel.: 145-89-991-554; fax: 1
45-89-(Dijkstra et al., 1997). As there is a limit to the 991-525.
E-mail address: [email protected] (M.T. Sørensen). capacity of the single cell, the number of cells
determines the upper limit for the milk production and at weaning after a 4-week nursing period (25–28 capacity of the udder. The correlation between milk days). The piglet average daily gain (ADG) was production and mammary DNA content, which is an calculated for the period between litter size adjust-indirect measure of the number of cells, was reported ment and weaning. The piglets were not given any to be 0.34 to 0.60 in cattle (Tucker et al., 1973), and creep feed during the nursing period, but had free 0.75 in the rat (Knight et al., 1984). The main access to water.
objective of the present study was to determine
whether there is a similar relationship in the pig. 2.2. Recording of teat order
The piglets were fitted with ear tags on day 1 for
2. Materials and methods individual identification. Teat order was observed at an average of five sucklings on day 14 and day 21 of 2.1. Animals lactation. For easy identification, the piglets were marked with numbers on their backs. Teat order was The animal material comprised seven sows and defined as stable if the piglet remained at the same their litters from the herd at ‘Grønhøj’, a facility teat during the milk letdown for all or all but one of owned by the Danish Slaughterhouses. Three of the the sucklings observed per day at the 2 days of sows were primiparous, while four were multiparous observation. The observations determined a total of (three third parity and one fourth parity). The sows 56 stable teat–piglet combinations (i.e. 38 with a were Landrace3Yorkshire crosses except for one complete teat order, one piglet had an incomplete purebred Yorkshire. They were fed a cereal soybean- suckling on day 14, nine piglets had an incomplete based diet (Table 1). Daily feed allowance was 1.9 suckling on day 21, and eight piglets had an incom-kg from week 1 to week 11 of gestation, 3.3 incom-kg from plete suckling on both days). In most of the cases, week 12 to week 14 and 2.8 kg from week 15 to the suckling became incomplete because the piglet week 16. The last 2 days before expected farrowing, did not rise to suckle. Only data from the 56 teat– feed was reduced to 2.0 kg per day. After farrowing, piglet combinations with a stable teat order were the sows were fed ad libitum. included in the analyses (77% of the weaned piglets).
Litter size was adjusted to 10 to 12 piglets within
24 h from farrowing. The piglets were weighed 2.3. Dissection of the udder individually after litter size adjustment (start weight)
The sows were weaned from the piglets at 7.00 h, transported to the slaughterhouse at Research Centre
Table 1 1
]
Foulum, and slaughtered 12 to 2 h after weaning. Feed composition in the lactation period
After scalding, the udder and the first muscle layer
Ingredients dorsal to the udder were excised from the carcass,
Wheat, % 39.6 split in left and right halves and stored at 2208C.
Barley, % 27.0 The frozen half udder was cut into 1.0–1.5 cm
Soya bean meal, toasted, % 14.8
thick slices with a band saw. Initially the udder was
Oats, % 5.0
cut through the fourth gland at an angle
perpen-Sunflower meal, % 5.0
dicular to the longitudinal direction. Then the slices
Animal fat, % 3.0
Dicalcium phosphate, % 1.9 were cut along the longitudinal direction. The still Fish meal, % 1.5 slightly frozen slices were then separated at the gland
Sugar beet molasses, % 1.0
boundaries either by breaking or cutting the slice.
Calcium carbonate, % 0.6
This separation was difficult at times, due to
ill-Sodium chloride, % 0.4
defined boundaries between the glands. Narrowings
Mineral and vitamin, % 0.2
ME, MJ / kg feed 13.5 in or under the skin, slight differences in colour, and Crude protein, g / kg feed 167 position of boundaries on adjacent slices were used
Lysine, g / kg feed 7.8
individual mammary glands was subsequently dis- incubated at 378C for 30 min. Fiveml SYBR Green sected from the adjacent tissue (skin, fat and muscle). II solution diluted according to the instructions from The mammary tissue was weighed and stored at the supplier were then added. After 5 min, excitation
2208C. was performed at 468 nm and emission measured at During dissection there was an average weight 520 nm. The emission from the aliquots with RNase loss of 5.5% due to the use of the band saw. The was considered unspecific background. Thus, the presented data have been adjusted for this weight difference between the measurements of the aliquots loss by adding 5.5% to each gland. The initial cut with or without RNase was considered specific, and through the fourth gland caused a small weight loss the RNA content was estimated from the standards. (anticipated to be less than 1%) for which no From this estimate, the RNA concentration adjustment was made. (RNAconc) and total amount of RNA of individual glands (RNAtotal) were calculated. Level differences 2.4. Fat, DNA and RNA analyses between microtitre plates were corrected by means of
the control samples. The frozen mammary tissue of individual glands
was cut into pieces, minced in a meat grinder and 2.5. Statistical method mixed thoroughly.
A sample of the minced tissue was analysed for Model I or a reduced version of this model was diethyl ether extractable fat after hydrolysis with used in the analyses of the effect of parity and gland boiling 3 M HCl according to the method of Stoldt position on the data in Table 3. The REML meth-(1952). odology of the SAS procedure PROC MIXED was
For DNA analysis, a sample of the minced tissue used (SAS, 1996). was homogenised with a polytron in PBS buffer and
analysed by the fluorometric method of Labarca and Y 5m 1 a 1 b 1 g 1 h*V 1U 1e (I) lspg p l pl lspg ls lspg Paigen (1980). From this measure, the DNA
con-centration (DNAconc) and total amount of DNA of where Y is response variable; m is the general lspg
individual glands (DNAtotal) were calculated. mean;a is the effect of position p; b is the effect
p l
RNA was measured fluorometrically with SYBR of parity l;g is the position3parity interaction;his pl
Green II dye (Molecular Probes, S-7568). The regression coefficient; V is the piglet start weight; lspg
method by Schmidt and Ernst (1995) to measure U is the random effect of the individual sow; e is
ls lspg
RNA in DNA-free samples was modified in order to the random residual effect; l: parity (primi- or enable measurement of RNA in DNA-containing multiparous); s: sow number within parity (1 to 7); samples, since both DNA and RNA enhance the p: position (1 to 3, see definition in Table 3); g: fluorescence of SYBR Green II. A sample of the piglet number within sow (1 to n, where n is minced tissue was homogenised with a polytron in between 5 and 10).
PBS buffer and diluted in TE buffer (10 mM Tris, 1 The complete model I was only applied for piglet mM EDTA, pH 7.0). A sample of a control tissue ADG. For the other response variables, the inter-pool (a mix of tissue from all sows) was also action term and piglet start weight were not signifi-included and treated as the other samples. Four 100 cant (P.0.05) and thus excluded from the model.
ml aliquots of each sample were transferred to a The partial correlations between mammary gland microtitre plate. Five ml TE buffer were added to compositional traits (amount of mammary tissue, two of the aliquots while 5 ml DNase-free RNase DNAtotal, RNAconc, RNAtotal, RNA / DNA ratio) solution (1mg / 10ml, Boehringer Mannheim cat. no. and piglet average daily gain given piglet start 1119915) was added to the other two aliquots. Each weight were calculated from a multidimensional microtitre plate also included a blank (TE buffer) and covariance component model (model II) using the RNA standards (200 to 2000 ng / ml) (RNA from SAS procedure PROC MIXED (SAS, 1996). Bakers yeast, Sigma R-6750) in duplicates. After
Table 2 DNAtotal was also calculated from a model similar General production data to model II, but based on these two variables.
Parity
Primiparous Multiparous
3. Results
Litter size, live born piglets 7.3 9.5 Litter size, after adjustment 10.3 11.3
General production results are shown in Table 2. Litter size, weaned piglets 10.1 10.8
Age at weaning, days 26.9 26.8 The high piglet start weight was due to inclusion of a,b
Piglet start weight, kg 1.8 2.0 piglets which were several days old to litters with b
Piglet weight at weaning, kg 7.0 8.3
less than ten piglets. Although the litter size is No. of piglets with stable teat order 8.3 7.7
relatively small, the production results are within the b
Includes only piglets with a stable teat order. normal range indicating that the animal material is a
Because of adjustment of litter size, piglets older than 1 day
representative. may be included.
Mammary gland size (amount of mammary tissue where Ylsg is the 3-dimensional observation (com- and total DNA) was higher in multiparous than in prised of the mammary gland compositional traits primiparous sows, whereas there was no significant and piglet ADG, and piglet start weight as a effect of parity in the other compositional traits covariate) on piglet g from sow number s within (Table 3). The concentration and amount of mam-parity l; Uls is the random effect of the individual mary RNA as well as mammary RNA / DNA ratio sow; elsg is the random residual effect. were dependent on gland position, i.e. highest in the Parity was included in the model when it was front glands, intermediate in the middle and lowest significant at P-level 0.05. in the rear glands. Average daily gain of the piglets The correlations between mammary gland traits was of the same magnitude regardless of the position and piglet start weight were calculated from a model of the gland they suckled in primiparous sows. In similar to model II with Ylsg a 2-dimensional ob- multiparous sows, growth rate was highest in the servation consisting of mammary gland composition- piglets suckling the front teats, intermediate in the al traits and piglet start weight. The correlation piglets suckling the middle teats and lowest in the between the amount of mammary tissue and piglets suckling the rear teats.
Table 3
Mammary gland compositional traits and piglet growth rate (ADG) in relation to parity and gland position*
Parity Primiparous Multiparous S.E.M. P-value
1
Gland position Front Middle Rear Front Middle Rear Range Parity Position
Number 10 10 5 11 11 9
a a a b b b
Tissue, g 504 481 495 658 635 648 43–51 0.01 0.71
FATconc, mg / g 76.5 75.5 83.2 82.0 81.1 88.7 8.7–10.1 0.67 0.07
FATtotal, g 39.2 36.7 42.2 54.2 51.6 57.1 6.7–7.8 0.14 0.25
DNAconc, mg / g 2.34 2.36 2.29 2.33 2.35 2.29 0.05–0.06 0.92 0.65
a a a b b b
DNAtotal, g 1163 1124 1113 1539 1500 1489 108–127 0.02 0.69
cde cde ab bcd bc a
RNAconc, mg / g 13.6 12.8 10.4 12.0 11.2 8.8 0.8–1.0 0.15 ,0.001
bcd bc a de cde ab
RNAtotal, g 6868 6152 4870 7670 6955 5672 464–572 0.16 0.003
de cde ab bcd bc a
RNA / DNA ratio 5.82 5.40 4.51 5.17 4.75 3.85 0.34–0.41 0.15 0.001
2
Piglet start wt. , kg 1.79 1.75 1.83 2.01 1.91 2.03 0.18–0.33 – –
abc ab abcd d bcd a
Piglet ADG 222 218 230 274 244 205 16–21 NA NA
LSMeans, P-values and Standard Error of Mean from model I. 1
Gland position (front5pair 1 and 2; middle5pair 3 and 4; rear5pair 5 to 7). 2
Means and S.D. of piglet start weight.
NA: Not applicable because the Parity3Position interaction was significant (P50.007) for ADG. a,b,c,d,e
Table 4
Correlations between mammary gland traits, piglet ADG and piglet start weight Mammary tissue trait
Amount DNAtotal RNAtotal RNAconc RNA / DNA
a 1
Piglet ADG 0.35* 0.41* 0.31*** 0.28 0.22
b
Piglet start weight 0.25 0.33 0.14 20.24 20.18
1, P,0.10; *, P,0.05; ***, P,0.001. a
Conditioning on piglet start weight in model II. b
Parity significant at P-level 0.05 and included in model II.
Fig. 1. The relationship between average daily gain of individual piglets and the DNA content of the mammary gland suckled by individual piglets (correlation50.41).
Average daily gain of the piglets was positively et al., 1984), although in these species the relation-correlated to the amount of mammary tissue (0.35), ship was based on the whole udder instead of total mammary DNA (0.41) and total mammary individual mammary glands.
RNA (0.31), while the correlation to mammary RNA In the present experiment, the growth rate of the concentration (0.28) and the RNA / DNA ratio (0.22) offspring was used as the measure of milk yield, as did not reach significance (Table 4 and Fig. 1). was also the case in the above-mentioned experi-A high correlation was found between the gland ments with rodents. However, since milk yield weight and DNAtotal (r50.94). There were no measured by the weigh–suckle–weigh method and significant correlations between DNAconc and gland piglet growth rate is highly correlated (Lewis et al., weight or between DNAconc and DNAtotal (data not 1978; Noblet and Etienne, 1989), the correlation to shown). mammary gland size would probably be of the same magnitude regardless of the method used to measure milk yield.
per gram tissue) and fat content (approximately 8%) unaffected by birth weight in first parity sows, while in mammary tissue also contributes to these findings. in older sows the larger piglets select the anterior The concentration of DNA (and also of RNA) in glands. This tendency increases with parity (Dyck et lactating mammary tissue agrees very well with the al., 1987). The finding that RNA concentration and values found by Li and Hacker (1995) in lactating total RNA content were highest in the front glands, sows and by Tucker et al. (1973) in lactating dairy intermediate in the middle glands and lowest in the cows. rear glands suggests that gland activity and thus Because the amount of DNA is constant at approx- synthesis of milk may follow a similar pattern. imately 6 pg per cell (Lehninger, 1975), the correla- However, it remains unexplained why growth rate of tion between mammary DNA and piglet ADG piglets from multiparous sows, but not from indicates that milk yield is correlated to the number primiparous sows follows a similar pattern.
of milk-producing cells. The correlation between mammary RNA and piglet ADG was of a lower
magnitude indicating that mammary cell number is 5. Conclusion
more determining for milk yield than cell activity.
This is in agreement with Knight et al. (1984) who The existence of a correlation between gland size showed that increased mammary tissue cell number and milk yield indicates that female breeding stock accounted for 75% of the milk yield increase in the should be reared in a way that facilitates mammary lactation period in rats, whereas 25% was accounted growth. However, research is needed to define for by increased cell activity. rearing recommendations.
In our hands, piglets require approximately 3.5 kg milk measured by the weigh–suckle–weigh method
per kilogram weight gain (Sørensen et al., 1998). If Acknowledgements this figure is applied to the data in Table 3, it can be
calculated that 1 g of wet mammary tissue produces We wish to thank The Federation of Danish Pig 1.1 to 1.6 g of milk. This is within the range reported Producers and Slaughterhouses for the animal ma-in guma-inea pigs, i.e. 2.1 g milk per gram wet weight at terial.
peak lactation and 0.2 g at the end of lactation (Sheffield and Anderson (1985).
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