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Articles

Ascorbic Acid Synthesis in Fetal and Neonatal Pigs and in Pregnant and Postpartum Sows^{1 ,2}

San Ching^*, Donald C. Mahan^*3, Joseph S. Ottobre^* and Konrad Dabrowski

^* Department of Animal Sciences, School of Natural Resources, The Ohio State University and The Ohio Agricultural Research and Development Center, Columbus, OH 43210-1094

³To whom correspondence should be addressed. E-mail: mahan.3{at}osu.edu.

	ABSTRACT

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The ontogeny of ascorbic acid synthesis and its concentration in fetal pigs from mid- to late gestation, and the effect of birth order and premature or normal delivery ages were evaluated. In Experiment 1, fetal pigs were collected from three sows at 60, 80, 100, 107 and 111 d of development. Liver L-gulono--lactone oxidase (GLO) activity and ascorbic acid concentration were measured. High liver GLO activity in fetal liver occurred at 60 d but declined as pregnancy advanced (P < 0.01), whereas ascorbic acid concentration increased (P < 0.01). Experiment 2 evaluated ascorbic acid synthesis and concentration in neonates born early (1st and 2nd) or late (7th and 8th) in the birthing sequence, or when born 2 d prematurely vs. the normal delivery age. Pigs born early in the birthing sequence (P < 0.01) and those born at the natural delivery age (P < 0.05) had higher liver ascorbic acid concentrations, but liver GLO activity did not differ among groups. Sows were killed at each period; liver GLO activity was constant during gestation but increased postpartum (P < 0.01). Liver ascorbic acid concentration was constant during gestation, except for a decline during late gestation, and increased postpartum (P < 0.05). These results suggest that more ascorbic acid was transferred from the dam to the fetuses as pregnancy advanced, possibly suppressing fetal GLO activity. Thus, fetal liver GLO activity was the primary source of ascorbic acid during early fetal development, but more fetal ascorbic acid was transferred from the dam during later pregnancy.

KEY WORDS: • L-gulonolactone oxidase • ascorbic acid • gestation • pigs

	INTRODUCTION

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Ascorbic acid is present in the tissues of fetal pigs from d 55 to 110 of gestation (1 ,2) . The high 14:1 ratio of fetal to sow plasma ascorbic acid concentration present during late pregnancy suggests that ascorbic acid is actively transported across the placenta (3) . Braude et al. (4) subsequently suggested that the synthesis of ascorbic acid was established in the young pig by 1 wk of age. It has therefore been presumed that because of the high colostrum and milk ascorbic acid concentration, an ample supply of the vitamin was available to the young pig before it was required to synthesize the vitamin.

The previous studies, however, determined ascorbic acid synthesis indirectly by measuring increasing tissue ascorbic acid concentrations or its excretion in urine (1 ,3 ,4) . L-Gulono--lactone oxidase [EC 1.1.3.8] (GLO)⁴ (4) is necessary for the biosynthesis of ascorbic acid and converts L-gulono--lactone to L-keto-gulono--lactone, whereupon L-ascorbic acid is produced through isomerization (5 ,6) . This enzyme is missing in primates and humans but is present in pigs and other species that synthesize the vitamin. The measurement of this enzyme, however, should more precisely reflect the synthesis of ascorbic acid than the tissue concentration of the vitamin.

The lowered blood supply to the fetuses during the birthing process has been shown to produce a hypoxic condition in neonatal pigs (3) . It has been reported that fetal serum, kidney, muscle and adrenal gland ascorbic acid concentrations were lowered upon birth (3) . Because swine are a litter-bearing species, and the parturition process generally takes several hours for completion, it is probable that pigs born later in the birthing sequence may have more hypoxic stress that may ultimately affect their ascorbic acid status.

Prostaglandin F₂ (PGF₂) has been used in pregnant sows to induce the birthing process and is frequently administered in commercial swine units 2–3 d before farrowing. The effect of premature delivery, albeit only a few days, on the neonatal ascorbic acid status is unknown.

One of our studies evaluated the ontogeny of liver GLO activity and subsequent tissue ascorbic acid concentration in fetal pigs from 60 d postcoitum to late gestation. Another experiment elucidated the effect of pigs born early or at their normal delivery age, and examined the effect of birth order on the ascorbic acid status of the neonate.

	MATERIALS AND METHODS

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General.

The 21 sows (14 Yorkshire x Landrace, 4 Duroc, and 3 Yorkshire) used in these two experiments were obtained from the Ohio State University swine research herd (Columbus, OH). In Experiments 1 and 2, sows were fed a 14 g/100 g crude protein (CP) corn-soybean meal gestation diet and a 18 g/100 g CP lactation diet, respectively, both fortified to meet NRC (7) nutrient recommendations. Neither diet was supplemented with ascorbic acid. All diets were mixed from grains and ingredient sources at the feed research mixing facility (Wooster, OH). Sows for both experiments were housed in groups of six or seven per gestation pen in complete confinement facilities at the Ohio State swine farm (Columbus, OH) in partially slotted (20%) concrete-floored pens that provided a minimum 1.25 m² floor space per pig. Overhead heaters and air bags delivered heated and circulating air as needed to maintain comfort. Sows were fed once daily in individual gestation crates (2.1 x 0.53 m) at 2.1 kg. The sows used in Experiment 2 were housed in the same gestation facility as those in Experiment 1, but placed into individual farrowing crates (2.1 x 0.67 m) at 109 d postcoitum. They were fed their gestation diet at 2.1 kg/d until farrowing. Upon farrowing they were fed the lactation diet at 2.5 kg/d, but the ration was cumulatively increased by 1 kg/d. Both experiments were conducted during the same time frame and the sow data for the two experiments were subsequently combined. Pig management and procedures used for tissue collection were approved by the university animal care committee.

Experiment 1.

The first experiment was a completely randomized design, conducted in three replicates and used a total of 15 sows. The GLO enzyme activity and ascorbic acid concentrations were measured in the liver and kidney of fetal pigs and their dams at five periods of development (60, 80, 100, 107 and 111 d) or postcoitum, respectively. Three sows were randomly assigned to each treatment group before the start of the experiment such that only one purebred was within each treatment group. Upon reaching the designated treatment day, pregnant sows were transported to the abattoir at the Ohio State University Meat Laboratory 1 h after consuming their daily ration. Sows were treated calmly but electrically stunned and killed by exsanguination within 30 min of arrival at the abattoir. Upon removal of the uterus, individual fetal pigs were weighed. The liver and kidney of three randomly selected fetal pigs from each sow were excised and weighed. Each tissue was divided and half was frozen in liquid N and stored at -80°C for the later determination of GLO activity; the remaining portion was frozen in liquid N and stored at -20°C for determining ascorbic acid concentration. Tissue samples of liver, kidney, spleen, adrenal gland, placenta, corpus luteum and mammary gland were collected from each sow, frozen in liquid N and stored in the same manner as the fetal tissue. The entire process for each sow and litter was completed within 40 min. The GLO enzyme activities were determined within 30 d of collection. Sow tissues from the 107-d period were lost and therefore not available for analysis.

Experiment 2.

This experiment was a 2 x 2 factorial arrangement of treatments in a split-plot design. The main plot evaluated pigs that were born prematurely (113 d) or at the normal (115 d) delivery age. Pigs born early (1st and 2nd) or late (7th and 8th) during the birthing sequence constituted the two birth orders and served as the subplot. To obtain pigs born prematurely, three sows were intramuscularly administered 200 mg of PGF₂ (Lutalyse, Upjohn, Kalamazoo, MI) at d 112 of gestation. These sows farrowed within 24 h and 2 d earlier (113 d) than the other set of three sows that were allowed to farrow at their natural time (115 d) postcoitum.

Immediately upon birth, neonatal pigs were placed in a warm container preventing them from consuming colostrum. Treatment pigs were electrically stunned and killed by exsanguination within 1 h of delivery. Samples of liver and kidney were collected and stored as indicated in Experiment 1 for the determination of GLO activity and ascorbic acid concentration.

Two sows administered PGF₂ and one that farrowed at the normal delivery age (115 d) were taken to the abattoir and killed 1-d postpartum as in Experiment 1. The remaining three sows were also killed at 5 d postpartum. Sow tissues (liver, kidney, spleen, adrenal gland, mammary gland, corpus luteum) were collected from each sow and stored as in the previous experiment.

Analytical procedures.

The measurement of GLO enzyme activity was based on a colorimetric procedure (8) adapted for swine tissue (9) . Ascorbic acid concentration was determined by the dinitrophenyl-hydrazine method (10) . Total ascorbic acid was measured at 524 nm by a multiwavelength spectrophotometer (DU-70; Beckman Instruments, Fullerton, CA). Tissue concentration of -tocopherol was measured by HPLC (11) using the sample preparation procedure outlined by Hatan and Kayden (12) .

The fetal pig data of Experiment 1 were analyzed as a completely randomized design (13) , whereas the neonatal pig data of Experiment 2 were analyzed as a split-plot design (13) by the General Linear Model procedure of SAS (14) . Probability values < 0.05 are reported. Because ascorbic acid concentrations, liver GLO activities and tissue -tocopherol concentrations of sows at 1 and 5 d postpartum were similar, these two data sets were combined and reported jointly. In the first experiment, the average value from the three fetal pigs was considered the experimental unit. Pig tissue ascorbic acid concentrations were averaged within each litter; the values were used to calculate the average pig and litter tissue ascorbic acid concentrations by multiplying the average value by the tissue weights of the fetuses in each litter. In Experiment 2, the 1st and 2nd pigs and the 7th and 8th pigs were averaged within each litter, with the mean of each group representing the experimental unit for the early and late delivered pigs, respectively.

	RESULTS

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Fetal pig ascorbic acid status.

Fetal liver GLO activity was highest at 60 d postcoitum and declined linearly (P < 0.01) to late pregnancy (Table 1 ). The decline, however, seemed to be more dramatic between 60 and 100 d postcoitum, and a plateau seemed to occur to 111 d of development. We found no GLO activity in the kidney of fetal pigs or in the placenta from 60 to 111 d of gestation (data not presented).

From 107 to 111 d of gestation, the concentration of ascorbic acid/g tissue declined in fetal liver and kidney (P < 0.01). When the ascorbic acid concentrations of these tissues were multiplied by their respective tissue weights and number of developing fetuses, the total ascorbic acid concentrations in the livers seemed to reach a plateau in the individual fetus or whole litter during the period from 107 to 111 d, but declined (P < 0.01) in the kidney. This implies that the rapid growth of fetal liver during this period was perhaps greater that the amount of ascorbic acid retained, which resulted in its lower relative concentration in the liver.

Pig birth order and premature and normal delivery.

There was no difference in pig liver GLO enzyme activity when pigs were born early (1st or 2nd) or late (7th or 8th) in the birth sequence (Table 2 ). Pigs that were also born 2 d prematurely (113 d) had liver GLO activity that did not differ from that of pigs born at the normal delivery age (115 d).

Pigs born 2 d early or from sows administered PGF₂ had lower liver ascorbic acid concentrations (P < 0.05) than pigs born at the normal delivery age, whereas kidney ascorbic acid concentrations did not differ between groups. It is possible that during the last 2 d of gestation, more maternal ascorbic acid was being transferred to the fetuses, and the additional time in utero resulted in higher liver ascorbic acid concentrations.

Sow ascorbic acid status.

Sow liver GLO activity was relatively constant during d 60 to 111 of pregnancy but increased upon parturition, resulting in an overall quadratic response (P < 0.01; Table 3 ).

View this table: [in this window] [in a new window]   Table 3. Sow liver L-gulonolactone oxidase (GLO) activity and tissue ascorbic acid and -tocopherol concentrations from d 60 to 111 of gestation (Exps. 1 and 2)

Ascorbic acid concentration in the sow’s adrenal gland and corpus luteum was higher than in other maternal tissues. Ascorbic acid increased markedly in the corpus luteum between d 60 and 80 postcoitum, declined by 111 d and continued to decline after parturition in a quadratic manner (P < 0.01). A similar pattern (P < 0.01) was evident for the spleen in which the ascorbic acid concentration was highest at d 60 and then declined by d 111 of gestation. The postpartum spleen ascorbic acid concentration was similar to the prepartum value. Placenta ascorbic acid concentration increased to d 100 of pregnancy and then seemed to reach a plateau or decline slightly, resulting in a quadratic response (P < 0.01).

The -tocopherol concentration in the adrenal gland of the sows increased linearly (P < 0.05) from d 60 of gestation through the postpartum period. In contrast, the -tocopherol concentration in the corpus luteum declined numerically during gestation but increased markedly after the sows farrowed, resulting in an overall quadratic response (P < 0.05).

From 111 d postcoitum to the postpartum period, the ascorbic acid concentration in sow mammary gland was substantially lower after sows farrowed (P < 0.01). The incorporation of ascorbic acid into the mammary fluids and its subsequent removal by the nursing pigs likely account for this decline.

	DISCUSSION

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Our experiments demonstrated that fetal pigs have a high capability to synthesize ascorbic acid during their early developmental stages, but liver GLO activity declined dramatically as pregnancy advanced. Our results further indicate that there was a large increase in the quantity of ascorbic acid retained in the fetus during late gestation. Although fetal synthesis of ascorbic acid during that period cannot be discounted, our results suggest that the increasing fetal retention was probably due more to the transfer of ascorbic acid from the dam than to fetal synthesis. It was reported previously that pig fetal liver GLO activity was present at d 84 of gestation (15) . Activity of the GLO enzyme and a high concentration of ascorbic acid in the liver and(or) kidney have been demonstrated in other species (16) , but we found GLO activity only in the liver of the pigs. The increasing ascorbic acid concentration in fetal pig tissue may have been responsible for suppressing fetal liver GLO activity with advancing pregnancy. Ascorbic acid is involved in the hydroxylation reaction of collagen synthesis (17) , and fetal pigs would be expected to have a high requirement during the early developmental period. Our results therefore suggest that during early development, fetal pigs require more ascorbic acid than can be provided from maternal transfer and that fetal synthesis is high during this period. However, once maternal transfer of ascorbic acid increases, the synthesis of ascorbic acid by the fetus is reduced. Maternal ascorbic acid therefore seems to be the primary source of ascorbic acid to the fetuses during the latter but not during the early part of pregnancy. Our interpretation concerning the beginning of ascorbic acid synthesis in the pig, however, differs considerably from that of Braude et al. (4) , and Brown et al. (3) who concluded that ascorbic acid synthesis in young pigs begins postnatally.

Sow liver GLO activity remains relatively constant during gestation, but liver ascorbic acid concentration declines during late gestation. The declining concentration of ascorbic acid probably reflects more of the vitamin being transferred to the mammary and fetal tissues as pregnancy advances. Upon the onset of milk secretion, sow liver GLO activity increased. Because colostrum and milk both have a high concentration of ascorbic acid that is removed by the nursing pigs (18) , the decline in sow mammary and other sow tissue ascorbic acid concentrations undoubtedly reflects its diversion into the milk supply.

In pregnant sows, the adrenal gland and corpus luteum had higher ascorbic acid concentrations than other maternal tissues. Wegger and Palludan (19) studied ascorbic acid metabolism in pigs and suggested that some endocrine glands such as the adrenal have a high priority for ascorbic acid utilization, resulting in its higher concentration. Petroff et al. (20) indicated that at 40 d postcoitum, the ascorbic acid concentration in the corpus luteum was approximately eight times higher than in the follicle before ovulation. They suggested that the corpus luteum retained ascorbic acid to maintain progesterone synthesis and to prevent oxidative damage to this tissue during pregnancy. Our results showed that ascorbic acid increased in the corpus luteum to d 100 of gestation, declined by d 111 postcoitum and then declined further after the sows farrowed. Others (21 ,22) had previously indicated that rat corpus luteum ascorbic acid concentration was reduced after exogenous PGF₂ administration. Ascorbic acid in the corpus luteum may be used as an antioxidant by preventing the formation of lipid peroxides (23) . Exogenous PGF₂ has been shown to deplete ascorbic acid from the corpus luteum by releasing the vitamin into the blood (24) . These last-mentioned authors also suggested that the depletion of ascorbic acid was an early event associated with luteal regression.

The administration of PGF₂ has also resulted in the accumulation of reactive oxygen species within the corpus luteum (25) . The corpus luteum may, therefore, oxidize ascorbic acid and thereby release less ascorbic acid through blood circulation to the fetal pigs. Ingermann et al. (26) demonstrated that dehydroascorbic acid is effectively transported by a Na-independent monosaccharide transporter in a human placenta. Pig epitheliochorial placenta has more layers and is therefore thicker than human hemochorial placenta, and this may have reduced the transport of ascorbic acid to fetal pigs. This may be a reason why fetal pigs must synthesize ascorbic acid during the early development period.

Fetal ascorbic acid has been shown to be metabolized during the birth process, with the ascorbic acid source originating from the adrenal gland of the fetus (27) . Exogenous PGF₂ administered to sows to induce the birthing process as in our experiment may therefore increase the amount of adrenal ascorbic acid released from both the birthing dams and fetuses.

The farrowing process has been shown to be stressful to both dams and fetuses (27) . A high correlation exists between ascorbic acid concentration in the adrenal gland and fetal blood oxygen (3) . These authors also suggested that the farrowing process produced hypoxia in fetal pigs from frequent uterine contractions during birthing. Consequently, this could result in a lowered tissue ascorbic acid status with prolonged parturition or later births. Farrowing stress is undoubtedly more severe on pigs that are born later in the delivery process. Our experiment indicated that pigs born late in the birthing sequence indeed had a lower liver ascorbic acid concentration. The administration of PGF₂, however, seems to have had no effect on the neonate’s ability to synthesize ascorbic acid, but it did affect their liver ascorbic acid concentration, which was lower in pigs from sows induced to farrow early (113 d) compared with those that farrowed at the normal (115 d) delivery age. Liver ascorbic acid seems to be more labile than that from the kidney in both young pigs and sows. Our results suggest that although tissue ascorbic acid concentration seemed to be affected by premature birth and prolonged parturitions, these factors did not seem to affect the ability of neonatal pigs to synthesize ascorbic acid.

	ACKNOWLEDGMENTS

 
Appreciation is expressed to K. Mays and A. C. Ottobre for animal care, data and tissue collection, R. Moreau, F. Cihla and M. Watts for laboratory assistance, and B. Bishop for statistical analysis.

	FOOTNOTES

 
¹ Research support was provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University.

² Supported in part by Hoffman La-Roche, Paramus, NJ.

⁴ Abbreviations used: CP, crude protein; GLO, L-gulono--lactone oxidase; PGF₂, prostaglandin F₂ .

Manuscript received August 21, 2000. Initial review completed October 5, 2000. Revision accepted March 30, 2001.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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24. Petroff B. K., Ciereszko R. E., Dabrowski K., Ottobre A. C., Pope W. F., Ottobre J. S. Depletion of vitamin C from pig corpora lutea by prostaglandin F₂-induced secretion of the vitamin. J. Reprod. Fertil. 1998;112:243-247[Abstract/Free Full Text]

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart 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 HighWire Citing Articles via Google Scholar Google Scholar Articles by Ching, S. Articles by Dabrowski, K. Search for Related Content PubMed PubMed Citation Articles by Ching, S. Articles by Dabrowski, K.