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J. Anim. Sci. 2002. 80:1759-1770
© 2002 American Society of Animal Science

Fetal development in the pig in relation to genetic merit for piglet survival1

J. I. Leenhouwers*, E. F. Knol{dagger}, P. N. de Groot*, H. Vos* and T. van der Lende*,2

* Animal Breeding and Genetics Group, Wageningen Institute of Animal Sciences, Wageningen University, Wageningen, The Netherlands and and {dagger} IPG, Institute for Pig Genetics B.V., Beuningen, The Netherlands

2 Correspondence:
P.O. Box 338, 6700 AH Wageningen, The Netherlands (phone: +31-317-482335; fax: +31-317-483929; E-mail:
tette.vanderlende{at}alg.vf.wag-ur.nl).


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The objective of this study was to investigate if litters with different genetic merit for piglet survival differ in late fetal development. In total, 507 fetuses from 46 litters were delivered by Caesarean section at, on average, d 111 of gestation. All litters had known estimated breeding values for piglet survival (EBVps). The obtained range of EBVps of the litters was continuous, and the difference between litters with the lowest and highest EBVps was 16.4%. Analysis of relationships between fetal characteristics and EBVps was performed with litter averages, using linear regression analysis with inclusion of EBVps as a covariate. An increase in EBVps of the litter was associated with decreases in average placental weight (P = 0.01) and within-litter variation in placental weight (P = 0.02), and an increase in average placental efficiency (P = 0.08). Average fetal length decreased with increasing EBVps (P = 0.04), but weights of liver (P = 0.02), adrenals (P = 0.0001), and small intestine (P = 0.01) showed relative increases with increasing EBVps. Average serum cortisol concentrations increased with increasing EBVps (P = 0.0001), but the other blood characteristics (hematocrit, glucose, fructose, albumin, estradiol-17ß) were not related to EBVps. Glycogen concentrations in liver (P = 0.07) and longissimus dorsi muscle (P = 0.04) and total liver glycogen content (P = 0.05) increased with increasing EBVps, whereas heart glycogen concentration decreased with increasing EBVps (P = 0.005). The percentage of carcass fat increased with increasing EBVps (P = 0.05). Relationships of relative liver weight, relative small intestinal weight, and liver and muscle glycogen levels with EBVps were absent after adjustment for differences in cortisol levels between litters. The observed differences in fetal development in relation to EBVps suggest a higher degree of physiological maturity in litters with high EBVps. Differences in fetal cortisol most likely accounted for most of these maturational differences. The results imply that selection for improved piglet survival will lead to slightly smaller piglets that nevertheless have an improved ability to cope with hazards during birth or within the first days of life.

Key Words: Animal Breeding • Breeding Value • Fetal Development • Perinatal Mortality • Pigs • Placenta


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Piglet survival from onset of farrowing until weaning can be increased by genetic selection, since considerable genetic variation exists for this trait (Van Arendonk et al., 1996; Knol et al., 2002). Increased survival of piglets with a higher genetic merit for survival cannot be explained by differences in the progress of farrowing or early postnatal piglet behavior (Leenhouwers et al., 2001). Therefore, we hypothesized that the biological background of genetic differences in piglet survival might be found in differences in late fetal development that are related to the ability of piglets to adapt to the various changes associated with transition from intrauterine to extrauterine life. The degree of late fetal development and maturation is an important predisposing factor for stillbirth and preweaning mortality and involves characteristics like placental functioning, functional maturity of vital organs, and availability of body-energy reserves (Randall, 1992; reviewed by Van der Lende et al., 2001).

The objective of this study was to investigate if litters with different EBVps differ in fetal development at d 111 of gestation. Fetal development was characterized by BW, body length, placental characteristics, organ characteristics, blood characteristics, glycogen reserves, and body composition.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
Animals, Housing, and Feeding.

This experiment was conducted strictly in line with the regulations of the Dutch law on the protection of animals. The gilts (n = 46) that were used in this study originated from a multiplier farm (Someren, The Netherlands) and were transported to the experimental accommodation "De Haar" of Wageningen University, The Netherlands between the ages of 11 and 20 wk. Upon arrival at the experimental accommodation, gilts were housed in groups of five, according to BW. After their arrival, all gilts were fed 0.9 to 1.5 kg/d of a starter diet (per kg: 13.8 MJ of ME; 167 g of CP; 10.0 g of lysine) until they reached the age of 15 wk. Beyond this age, they received, depending on body condition, up to 2.3 kg/d of a rearing sow diet (per kg: 12.9 MJ of ME; 155 g of CP; 8.0 g of lysine). From the age of 6 mo onward, gilts were checked daily for estrus with a vasectomized boar. At second, third, or fourth estrus, gilts were artificially inseminated twice on consecutive days with semen of one of 14 different boars. Gilts that returned to estrus after insemination were inseminated again. Three months after the start of estrus check, seven gilts did not show a natural estrus. For these gilts, estrus was induced by administration of PG 600 (Intervet Nederland B.V., Boxmeer, The Netherlands). These gilts were inseminated at second estrus after induction. After insemination of the last gilt in a group of five, gilts were fed 2.3 kg/d of a gestational diet (per kg: 12.2 MJ of ME; 140 g of CP; 7.0 g of lysine).

Experimental Design.

All gilts were of the crossbred line D12 of TOPIGS breeding company (Vught, The Netherlands). Line D12 was produced by D2 dams mated by D1 sires. Line D1 was founded in 1968 and originates from different Piétrain populations. Since 1993, line D1 is selected mainly for litter size and piglet survival. Line D2 was founded in 1968 and originates from different Great Yorkshire and Large White populations. Since 1993, line D2 is selected on litter size and mothering ability. To inseminate the D12 dams, semen of boars of a sire line S of TOPIGS breeding company was used. Line S was founded in 1976, using selected animals from dam lines D1 and D2 to produce a specialized sire line. Line S was solely selected on growth, feed-intake, and backfat thickness until 1993, when piglet survival was added to the breeding goal.

Since 1993, TOPIGS breeding company has used a registration protocol on 12 of their farms. This registration protocol involves individual weighing of all pigs at farrowing (including stillborn pigs, but excluding mummified pigs). Crossfostering of piglets is registered with identification of the nurse sow, as are date and cause of death in the case of failed survival. From the data set that results from this registration protocol, estimated breeding values for piglet survival (EBVps) could be calculated by using an animal model, with direct (piglet) and nurse sow as animal effects. Heritabilities for the direct and nurse sow effects were 0.032 and 0.035, respectively, and the genetic correlation was 0.00. Piglet survival was defined as a binary trait, with a zero score for piglets dead before or at weaning, including stillborn piglets, and a score of 100 if alive at the day of weaning. Sex, birth weight of the piglets in classes of 100 g, and litter size were taken as fixed effects, while litter effect of the natural mother of the piglets was taken as an uncorrelated random effect. The model that was used for calculation of EBVps was described in more detail by Knol et al. (2002).

Breeding values for piglet survival of the gilts and boars were estimated, using information on their own survival record as a piglet and using information on survival records of related animals. For estimation of breeding values of the boars, information on their offspring was also used, thereby ignoring results obtained in this experiment. Estimated breeding values for piglet survival of the litters in this experiment were calculated as the average of the respective gilt and boar. Matings were done in such a way that a maximum contrast in EBVps of the litters was achieved. The obtained range of EBVps of the litters in this study was continuous, and the difference between litters with the lowest and highest EBVps was 16.4%. This indicates an expected phenotypic difference in piglet survival from onset of farrowing until weaning of 16.4% between those litters.

Data Collection Procedures.

In total, 507 fetuses from 46 litters were delivered by Caesarean section between d 110 and 112 of gestation. On the day of surgery, gilts were food-deprived, weighed, and subsequently anesthetized by i.m. injection of 20 mL Stresnil (Janssen Pharmaceutica N.V., Beerse, Belgium). Approximately 1 h before surgery, i.m. injections of 3 mL of dormicum (Roche Nederland B.V., Mijdrecht, The Netherlands) and 9 mL of ketamine (Eurovet Animal Health B.V., Bladel, The Netherlands) were administered. Gilts were ear-catheterized (Microflex, Instruvet, Amerongen, The Netherlands), and additional i.v. injections of ketamine and dormicum were administered during surgery when necessary.

As each fetus was removed from the uterus, approximately 10 mL of blood was collected from the umbilical vein and umbilical artery via a 21-gauge needle (Terumo Europe N.V., Leuven, Belgium) and a 10-mL syringe (Terumo Europe N.V.). In the smaller fetuses it was not always possible to collect 10 mL from both vessels. For every third fetus, starting with the first, samples of umbilical venous and arterial blood were immediately analyzed after collection for partial pressure of oxygen (pO2) and carbon dioxide (pCO2) by the I-STAT handheld blood analyzer (I-STAT Corporation, Princeton, NJ). Measurement of pO2 and pCO2 was performed to ascertain that fetuses would not get hypoxic during the surgery procedure. Blood samples were collected into ice-cooled tubes without additive, with EDTA-NaF additive (i.e., a glycolysis inhibitor), and with lithium-heparin additive. Tubes were placed on ice and centrifuged at 2,000 x g for 10 min at 4°C. Serum and plasma were stored at -20°C until further analysis.

After blood collection, surgical silk (Instruvet B.V., Amerongen, The Netherlands) with a numbered tag was attached to the umbilical cord. The umbilical cord was then cut at 1 cm of the fetal abdomen, allowing the tagged cord to retract into the uterus. Each fetus was subsequently tagged with a matching number, thus allowing individual matching of fetus and placenta. After the umbilical cord was cut, fetuses were euthanatized immediately by intracardial injection of a 0.5-mL mixture of a central nervous system narcotic, a paralytic agent, and a local anaesthetic (T-61; Hoechst Roussel Vet N.V., Brussels, Belgium).

Directly following euthanasia, fetuses were weighed and samples of heart (apex of cardiac ventricles), liver, and muscles including the longissimus dorsi and the biceps femoris muscles were collected. These samples were immediately frozen by immersion in liquid nitrogen and then stored at -80°C until they were analyzed for glycogen content. Heart and liver glycogen were determined for all individual fetuses. Based on average fetal BW of the litter, two average fetuses were selected for analysis of muscle glycogen. These fetuses were also used for analysis of carcass moisture, protein, fat, and ash content. After surgery, fetal crown-rump length was determined, and the remaining internal organs (lungs, stomach, spleen, kidneys, adrenals, and small intestine) were removed and individually weighed. Length of the small intestine was also measured.

After surgery, the gilt was euthanatized by i.v. administration of a lethal dose of T-61. Next, the uterus was removed and the uterine horns were opened longitudinally along the anti-mesometrial side. Placentae were collected by carefully detaching them from the endometrium. The umbilical cord was cut from each placenta at the point where the umbilical arteries diverge, and subsequently cord length was measured. After removal of the umbilical cords, placentae were individually weighed and their lengths were measured. Placental efficiency was calculated as the ratio fetal BW:placental weight.

Chemical Analytical Procedures.

To determine hematocrit values, freshly collected blood was spun down in capillaries in a hematocrit centrifuge at 11,330 x g. Venous and arterial plasma glucose concentrations were determined spectrophotometrically in triplicate with the glucose oxidase-peroxidase anti-oxidase method, using a commercial kit (GOD-PAP; Boehringer, Mannheim, Germany). Arterial plasma fructose concentrations were determined by radial immunodiffusion, as described by Roe (1934). Arterial plasma albumin concentrations were determined by RIA using a commercial kit (CEA, Gif, France). Arterial serum cortisol concentrations were determined by a solid-phase 125I RIA method (Coat-A-Count TKCO; Diagnostic Products Corporation, Los Angeles, CA) according to the description of the manufacturer. The limit of quantitation was 5.8 ng/mL, and the interassay coefficient of variation was 7.3% (n = 7). Arterial serum estradiol-17ß concentrations were estimated by a solid-phase 125I RIA method (Coat-A-Count TKE) according to the description of the manufacturer with slight modifications as described for the cow (Dieleman and Bevers, 1987). The limit of quantitation was 9.5 pg/mL, and the interassay CV was 13.3% (n = 7).

Glycogen concentrations in heart, liver, and muscle were determined by the method of Carroll et al. (1956). Glycogen was extracted from the tissue by homogenization with 5% trichloroacetic acid solution. Glycogen was precipitated from the extract by 95% ethanol and determined with anthrone reagent in a colorimeter at 620 nm.

For analysis of body composition, frozen carcasses were weighed, cut into pieces, and homogenized separately in a commercial butcher’s mincer. The homogenates were stored at -20°C in sealed plastic bags until they were analyzed in duplicate for moisture, protein, fat, and ash content. Moisture content was determined gravimetrically, after drying at 103°C for 4 h. Nitrogen content (N) was measured using the Kjeldahl method, and protein values were calculated as N x 6.28. Fat content was determined by petroleum-ether extraction. Ash was determined gravimetrically after incineration at 550°C for 3 h.

Statistical Analysis.

Stage of gestation at fetus removal was calculated as the difference between day of Caesarean section and day of second insemination. Mummified fetuses were excluded from all analyses. Nonfresh dead fetuses at the moment of Caesarean section were included in the calculation of total number of fetuses and average fetal BW, but excluded from all other characteristics. Litter averages and within-litter SD were calculated for all characteristics. Litter averages for body composition and muscle glycogen concentrations were calculated on basis of the two fetuses per litter that were analyzed for these traits.

All data were analyzed using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC). The following models were used to analyze relationships of body and placental characteristics (Model [1.1]Go), and blood characteristics, glycogen reserves, and body composition (Model [1.2]Go) with EBVps:


[1.1]


[1.2]

where Yij is the dependent variable; µ = overall mean; GLi = stage of gestation (i = 110 to 112); M = percentage males within the litter; TNF = total number of fetuses; EBVps = estimated breeding value for piglet survival of the litter; ABW = average fetal BW; and eij = residual error. The effect of EBVps was tested against the residual error term. Stepwise elimination of nonsignificant (co)variates (P > 0.05) was applied.

The following models were used to analyze relationships of relative liver and small intestinal weights (Model [2.1]Go) and glycogen reserves (Model [2.2]Go) with serum cortisol concentrations:


[2.1]


[2.2]

where Yij = dependent variable; µ = overall mean; GLi = stage of gestation (i = 110 to 112); C = serum cortisol concentration; C2 = quadratic cortisol term; ABW = average fetal BW; and eij = residual error. The quadratic cortisol term was removed from the model in case of nonsignificance (P > 0.10). Relationships of liver and small intestinal weights and glycogen reserves with EBVps were also analyzed after adjusting for differences in cortisol by inclusion of EBVps in Models [2.1]Go and [2.2]Go.

The relationship between organ weight (Y) and fetal BW can be described by the following power function (Huxley, 1924):


[3]

where a = the proportionality coefficient (the intercept at unity); and b = scaling coefficient. To investigate relationships of organ characteristics (organ weights and length of the small intestine) with EBVps, Equation 3Go was extended into Equation 4Go:


[4]

Equation 4Go was transformed into a linear form by taking the natural logarithm:


[5]

Parameter estimates and P-values for b1, b2, and b3 were obtained from Equation 5Go by the GLM procedure. The individual fetus was used as the experimental unit, and effects of EBVps, ln(BW), and the EBVps x ln(BW) interaction were tested against sow as an error term. The interaction EBVps x ln(BW) was nonsignificant (P > 0.10) for all organs and subsequently removed from the model. This resulted in the following Model [6]Go that was used to analyze relationships of organ characteristics with EBVps:


[6]

where Yijk = dependent variable; µ = overall mean; GLi = stage of gestation (i = 110 to 112); EBVps = estimated breeding value for piglet survival of the litter; BW = individual fetal BW; Sowj = sow effect (j = 1–46); and eijk = residual error. The effects of EBVps and ln(BW) were tested against Sowj as an error term. GLi was removed from the model if nonsignificant (P > 0.05). For comparison of fetal characteristics between litters with low, average, or high EBVps, litters were divided into three classes on basis of their EBVps. The LSMEANS per EBVps class were computed by the LSMEANS statement in Proc GLM in a model that only included stage of gestation as a fixed effect. Significant differences between LSMEANS were tested by inclusion of the PDIFF option in the LSMEANS statement.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
General

The average stage of gestation in this experiment was 111.1 d (SD = 0.8 d). The total number of fetuses per litter averaged 11.0 (SD = 2.8 fetuses), which included 0.1 nonfresh dead fetuses (SD = 0.3 fetus). Figure 1Go shows that fetal concentrations of venous O2 and arterial CO2 remained constant during the surgery procedure.



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  		Figure 1. Average venous blood partial pressure of oxygen ({blacksquare}) and arterial blood partial pressure of carbon dioxide ({square}) values measured for every third fetus during Caesarean section.

 
Relationships with EBVps

Body and Placental Characteristics. Relationships of body and placental characteristics with EBVps are presented in Table 1Go. Average body length decreased with increasing EBVps, whereas average BW was not related to EBVps. Fetuses of litters with high EBVps (mean EBVps = +7.9%) were on average 1.3 cm shorter than fetuses of litters with low EBVps (mean EBVps = -3.8%). Within-litter variation in BW and length were not related to EBVps. Average placental weight showed a decrease with increasing EBVps. Placentae of litters with high EBVps (mean EBVps = +7.9%) were on average 40 g lighter than placentae of litters with low EBVps (mean EBVps = -3.8%). Within-litter variation in placental weight also decreased with increasing EBVps. Placental efficiency tended to increase with increasing EBVps. Average umbilical cord length and within-litter variation in umbilical cord length were not related to EBVps.


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  		Table 1. Relationships of body and placental characteristics with EBVps of the littera
 
Organ Characteristics. Absolute and relative values of organ characteristics for all litters and for three EBVps classes are shown in Table 2Go. With the exception of adrenal weight, absolute values of organ characteristics tended to be lower in litters with high EBVps. Litters with high EBVps had higher relative weights of liver and adrenals, and relatively longer small intestines, but relatively lighter spleens than litters with low EBVps.


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  		Table 2. Absolute and relative values of organ characteristics for all litters and for three EBVps classesa
 
Relationships of organ characteristics with EBVps were calculated taking into account the existence of allometric relationships between organ characteristics and BW (Table 3Go). The 95%-confidence intervals for the values of b2 show a significant deviance from 1.0 for stomach weight, kidney weight, adrenal weight, and small intestinal length, thus indicating nonisometric relationships between these organ characteristics and BW. Significant positive estimates of b1 for weights of liver, adrenals, and small intestine indicate relative increases in these organ weights with increasing EBVps. Stomach weight tended to show a relative increase with increasing EBVps, whereas spleen weight tended to show a relative decrease with increasing EBVps. These values for b1 indicate that the liver, adrenals, small intestine, and stomach of a fetus with an EBVps of +5% will be 7.1%, 21.7%, 5.4%, and 4.3% heavier, respectively, than those of a fetus of the same weight but with an EBVps of -5%. In contrast, the spleen will weigh 6.1% less.


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  		Table 3. Regression coefficients and P-values for the model: ln(Y) = ln(a') + b1EBVps + b2ln(BW)a
 
Blood Characteristics. Average serum cortisol concentrations increased with increasing EBVps, whereas within-litter variation in cortisol levels was not related to EBVps (Table 4Go). Average serum cortisol levels and adrenal weights for litters with low, average, and high EBVps are shown in Figure 2Go. No relationships were found between other blood characteristics and EBVps.


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  		Table 4. Relationships of blood characteristics with EBVps of the littera
 


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  		Figure 2. Average adrenal weights ({blacksquare}) and serum cortisol levels ({square}) for litters with low (mean estimated breeding value for piglet survival [EBVps] = -3.8%), average (mean EBVps = +2.0%), and high EBVps (mean EBVps = +7.9%).

 
Glycogen Reserves and Body Composition. Regression coefficients and P-values of relationships of glycogen reserves and body composition with EBVps are presented in Table 5Go. Average total liver glycogen content and longissimus dorsi muscle glycogen concentration increased with increasing EBVps, whereas heart glycogen concentration decreased with increasing EBVps. Total liver glycogen content and longissimus dorsi muscle glycogen concentration of fetuses from litters with high EBVps (mean EBVps = +7.9%) were 8.1% and 6.2% higher, respectively, than of fetuses from litters with low EBVps (mean EBVps = -3.8%). Heart glycogen concentrations were 9.6% lower in fetuses from litters with high EBVps. Liver glycogen concentration tended to increase with increasing EBVps, and the glycogen concentration in biceps femoris muscle was not related to EBVps. Liver glycogen concentrations were positively correlated with longissimus dorsi muscle (r = 0.42, P < 0.0001) and biceps femoris muscle (r = 0.41, P < 0.0001) glycogen concentrations. There was an overall positive correlation between glycogen concentrations in the two muscle types (r = +0.60, P < 0.0001). Heart glycogen concentrations were not correlated with glycogen concentrations in liver, longissimus dorsi muscle, and biceps femoris muscle (P > 0.10). The average fat percentage of the carcasses increased with increasing EBVps. No relationships with EBVps were found for moisture, protein, and ash content of the carcasses.


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  		Table 5. Relationships of glycogen reserves and body composition with EBVps of the littera
 
Relationships with Cortisol

Small Intestinal Weight and Liver Weight. Relative small intestinal and liver weights increased with increasing serum cortisol levels (Table 6Go). After subtracting the total amount of liver glycogen from the liver weight, the residual relative liver weight was also positively related to serum cortisol. The positive relationships of liver and small intestinal weight with EBVps (Table 3Go) became nonsignificant (P > 0.10) after adjusting for differences in cortisol.


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  		Table 6. Relationships of relative small intestinal and liver weights and glycogen reserves with cortisol
 
Glycogen Reserves. Glycogen concentrations in liver, longissimus dorsi muscle, and biceps femoris muscle increased with increasing serum cortisol concentrations, as did the total amount of liver glycogen. The positive relationships of liver and muscle glycogen levels with EBVps (Table 5Go) became nonsignificant (P > 0.10) after adjusting for differences in cortisol. Figure 3Go shows that, in general, the higher serum cortisol levels of fetuses with high EBVps (mean EBVps = +7.9%) compared with fetuses with low EBVps (mean EBVps = -3.9%) were associated with higher liver glycogen concentrations. Some fetuses exhibited very high cortisol levels that were not associated with high liver glycogen concentrations. These high cortisol levels most likely reflected a situation of fetal distress or disturbed fetal development, as these fetuses either had a very low BW, an enlarged heart, or they were strangled by their own umbilical cord. Heart glycogen concentrations tended to decrease with increasing serum cortisol levels. The negative relationship between heart glycogen concentration and EBVps (Table 5Go) remained significant (P < 0.01) after adjusting for differences in cortisol.



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  		Figure 3. Relationship between liver glycogen concentration, and serum cortisol for fetuses (n = 159) with high estimated breeding values for piglet survival (mean EBVps: +7.9%) and fetuses (n = 165) with low estimated breeding values for piglet survival (mean EBVps: -3.8%).

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
The perinatal survival chances of a piglet mainly depend on its ability to cope with stresses experienced during farrowing and during the first days after birth (Pomeroy, 1960; Randall, 1978). This ability is not only influenced by environmental conditions, but also has a genetic component (reviewed by Rothschild and Bidanel, 1998; Knol et al., 2002). The genetic component of piglet survival consists of a maternal genetic component (genotype of the mother) and a direct genetic component (genotype of the piglet). Estimations of the direct genetic component of piglet survival were obtained by calculation of EBVps (Knol et al., 2002). The present study reports results of late fetal development in relation to EBVps of the litter.

Between d 90 and 110 of gestation, the fetus itself may be responsible for the increase in maternal-fetal nutrient exchange (Biensen et al., 1998). Increased fetal nutrient uptake is accomplished either by enlarging placental surface area or by increasing placental vascularity. In this study, the observed decreased placental weight, similar placental length, and tendency for increased placental efficiency with increasing EBVps suggest that fetuses with high EBVps employ the latter strategy. Variation in placental weight significantly decreased with increasing EBVps of the litter. Surprisingly, this decrease in variation in placental weight was not accompanied by a significant decrease in variation in fetal BW. This result can be explained by the absence of very heavy placentae in litters with high EBVps. Beyond a certain placental weight, fetal weight does not increase anymore, indicating that a maximum fetal growth potential has been reached (Van Rens and Van der Lende, 2000). In this study, this stage is reached at a placental weight of approximately 300 g (Figure 4Go). Placentae heavier than 300 g occurred mainly in litters with low EBVps, thereby inducing extra variation in placental weight that was not accompanied by extra variation in fetal BW.



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  		Figure 4. Relationship between fetal BW and placental weight for fetuses (n = 163) with high estimated breeding values for piglet survival (mean EBVps: +7.9%) and fetuses (n = 160) with low estimated breeding values for piglet survival (mean EBVps: -3.8%). The vertical line at a placental weight of 300 g indicates the approximate point where fetal BW does not increase anymore with increasing placental weight.

 
The negative trend of the relationship between fetal BW and EBVps and the significant decrease in fetal length with increasing EBVps indicate a trend for reduced piglet size with increasing EBVps. This might seem contradictory in terms of piglet survival, because low birth weight reduces both farrowing and preweaning survival chances (Sharpe, 1966; English and Wilkinson, 1982). The positive relationship between survival and BW is certainly true within litters, where it can be explained by the relative inability of low BW piglets to compete with heavier littermates for colostrum (England, 1974; reviewed by Fraser, 1990). However, the positive relationship between survival and BW does not always hold when analyzed across breeds or lines. For example, piglets from Meishan litters survive almost as well as piglets from Large White litters, despite the fact that Meishan average BW is some 450 g lower (Lee and Haley, 1995). Further, piglets from obese selection lines have lower birth weights than piglets from lean lines, but nevertheless 17% higher survival rates from birth to weaning (Mersmann et al., 1984). Several studies have indicated that a greater physiological maturity at birth, as suggested by differences in body and tissue composition, metabolic and hormonal state, and fat metabolism, may be responsible for the higher survival rates of lighter obese piglets compared with heavier lean piglets (Mersmann et al., 1984; Stone, 1984; Herpin et al., 1993). As will be explained below, results from this study also indicate that the earlier reported higher survival rates of piglets with high EBVps (Leenhouwers et al., 2001) may be explained by higher degree of physiological maturity at birth.

Total liver glycogen content and longissimus dorsi muscle glycogen concentration increased with increasing EBVps. Liver glycogen plays an important role in glucose homeostasis during farrowing and in the period before ingestion of adequate amounts of colostrum (Mersmann, 1974). Muscle glycogen reserves are the primary energy source for heat production in the period before colostrum ingestion (McCance and Widdowson, 1959; Le Dividich et al., 1998). Therefore, our results suggest that piglets with high EBVps may have a higher ability to maintain glucose levels during and after farrowing and may be better able to maintain body temperature in situations of late colostrum intake.

The observed decrease in heart glycogen levels with increasing EBVps was rather unexpected, since heart glycogen is thought to be related to the ability of fetal pigs, lambs, newborn rats, rabbits, and guinea pigs to withstand asphyxia (Dawes et al, 1959; Randall, 1979). However, considering that only about 0.5% of total body glycogen is present in the heart near term (Okai et al., 1978), it is possible that the contribution of heart glycogen to energy supply during anoxia is minimal compared with other sources.

The relative increase of small intestinal weight and the tendency for an increase in stomach weight with increasing EBVps may indicate a higher degree of gastrointestinal development in litters with high EBVps. This may be in line with a previously reported positive genetic correlation between postnatal weight gain (g/d) measured between 29 and 130 kg BW and the direct genetic effect for pre-weaning piglet survival (Knol et al., 2001).

In the same BW range of 29 to 130 kg, Knol et al. (2001) also reported a significant positive genetic correlation between backfat thickness and the direct genetic effect of preweaning survival. Our current results show that EBVps-related differences in body fat are already apparent at the end of gestation. Although the fetal carcass fat percentage in this study was low (0.72%), and mobilization of body fat reserves during starvation is supposedly very low (reviewed by Herpin and Le Dividich, 1995), body fat may play a role in preventing heat loss by increasing thermal insulation (Mount, 1964). Our results indicate a 0.0004% increase in carcass fat per 1% increase in EBVps, which corresponds to a relative increase of 9% in carcass fat between litters with the lowest (-5.91%) and highest (+10.47%) EBVps. It is doubtful that this increase in carcass fat percentage will contribute to a better thermal insulation, but nevertheless it may add to an overall higher maturity of piglets from litters with high EBVps.

In the pig, the weight and volume of the fetal adrenal gland show a pronounced change between d 105 to 113 of gestation (Lohse and First, 1981; Nicolle and Bosc, 1989). Fetal cortisol levels start to rise concomitantly with the increased adrenal growth from approximately d 105 of gestation (Randall, 1983; Silver and Fowden, 1989). Cortisol stimulates and regulates maturation and development of a wide range of organs that have important functions in assuring survival after birth (reviewed by Liggins, 1994). For example, cortisol stimulates liver and muscle glycogen deposition (Fowden et al., 1985; Randall, 1988), gluconeogenic enzyme activity (Fowden et al., 1995), and maturation of the lungs, gastrointestinal tract, and thyroid (Liggins et al., 1994; Sangild et al., 2000). In this study, adrenal weights and serum cortisol concentrations were much higher in litters with high EBVps. As expected, relative liver and small intestinal weights, and liver and muscle glycogen levels were positively related to serum cortisol levels. Relationships of liver and small intestinal weight and glycogen reserves with EBVps were absent after adjusting for differences in cortisol. This suggests that effects of EBVps on these characteristics were due to differences in cortisol concentrations.

In conclusion, the observed relationships between characteristics of late fetal development and EBVps suggest an increase in physiological maturity with increasing EBVps. Higher physiological maturity in litters with high EBVps was likely due to the higher average cortisol concentrations in these litters. Whether the increased cortisol levels in litters with high EBVps are the result of increased ACTH levels produced by the pituitary or increased sensitivity of the adrenals to ACTH is currently unknown, but will be investigated in future experiments.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
An increase in genetic merit for piglet survival is associated with changes in late fetal development which are probably due to differences in circulating fetal cortisol levels. Knowing that cortisol plays a major role in the preparation for the transition from intrauterine to extrauterine life, piglets with a higher genetic merit for piglet survival may have an improved ability to cope with hazards during birth and within the first days of life.


   Footnotes
 
1 This research was financially supported by The Netherlands Technology Foundation (STW). The authors gratefully acknowledge Veterinary Practice "Kortenoord" for carrying out the surgery procedures. The authors also thank the staff of the experimental accommodation "De Haar," and Kristina Reese, Birgitte van Rens, Aline van Genderen, Marcel Taverne, Bert van der Weijden, Herman Jonker, and Peter Zanders for their help in this experiment. Thanks to Steph Dieleman for determination of estradiol-17ß and cortisol concentrations, and to Meijke Booij for the glycogen determinations. Special thanks to Jean Le Dividich and co-workers at INRA, St. Gilles, France, for valuable advice and determination of fructose and albumin concentrations. Back

Received for publication September 12, 2001. Accepted for publication February 21, 2002.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


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