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© 2007 The American Society for Nutrition J. Nutr. 137:652-656, March 2007

Nutrient Requirements and Optimal Nutrition

Dietary L-Arginine Supplementation Enhances the Reproductive Performance of Gilts1

Ronaldo D. Mateo2, Guoyao Wu2,3,*, Fuller W. Bazer3, Jun C. Park4, Izuru Shinzato5 and Sung Woo Kim2–4,*

2 Texas Tech University, Lubbock, TX 79409; 3 Texas A&M University, College Station, TX 77843; 4 National Livestock Research Institute-RDA, Suwon 441-707, Korea; and 5 Ajinomoto Co., Inc., Tokyo 104-8315, Japan

* To whom correspondence should be addressed. E-mail: sungwoo.kim{at}ttu.edu or g-wu{at}tamu.edu.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Arginine is a common substrate for the synthesis of nitric oxide and polyamines that are crucial for placental angiogenesis and growth in mammals. This study was conducted to test the hypothesis that dietary L-arginine supplementation may improve reproductive performance of pregnant gilts. Fifty-two pregnant gilts with body weight (BW) of 166.3 ± 1.8 kg were housed individually in gestation crates. At d 30 of gestation, gilts were assigned randomly to corn-soybean-based diets supplemented with 1.0% L-arginine-HCl or 1.7% L-alanine (isonitrogenous control). Both diets contained 13.0 MJ metabolizable energy/kg and 12.2% crude protein and were fed to gilts at 1 kg twice daily during gestation. Backfat thickness and BW were measured and blood samples were obtained on 30, 70, 90, and 110 d of gestation. At d 110 of gestation, gilts were transferred to individual farrowing crates. The numbers of total piglets born and born alive, as well as birth weights of piglets, were recorded immediately after farrowing. Throughout the gestation, BW or backfat thickness of gilts did not differ between treatment groups. Plasma urea concentrations were lower in arginine-supplemented than in control gilts at d 90 (P < 0.010) and d 110 (P < 0.001) of gestation. Compared with the control group, arginine supplementation increased the number of pigs born alive by 22% (11.40 vs. 9.37, P = 0.032) and live litter birth weight of piglets by 24% (16.38 vs. 13.19 kg, P = 0.016). This exciting finding provides the first evidence for a marked increase of live-born piglets by 2 per litter through nutritional intervention in gilts.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Intrauterine growth retardation is a significant problem in both animal and human nutrition (1). Particularly, embryonic loss and fetal deaths during gestation account for 30 to 50% of the total number of fertilized ova (2,3), thereby limiting the number of piglets born at farrowing. Modern sows have higher fetal growth rates than those in the past breeds due to intensive genetic selection (4,5). However, higher fetal growth rates may require an increased provision of nutrients for supporting the metabolic needs of both the sow and her fetuses (6). Moreover, uterine and umbilical blood flow per fetus decrease as litter size increases (7,8), which can lead to an unequal delivery of substrates among fetuses. Further, larger fetal litter sizes may limit uterine capacity, which can decrease fetal growth, increase fetal death, and reduce litter size at birth (9–12).

Arginine plays multiple roles in animal metabolism by serving as a substrate for protein synthesis, an intermediate in the hepatic urea cycle, and a precursor for the synthesis of various important metabolic molecules, including nitric oxide (NO)6 and polyamines (13,14). Several studies have demonstrated a crucial role for NO in enhancing blood flow during ovine pregnancy (15–18), therefore increasing the delivery of essential nutrients from maternal to fetal blood. Polyamines are synthesized from ornithine via the arginase pathway and are important determinants of embryogenesis and placental growth (19–21). Available evidence shows that both polyamines and NO play key roles in angiogenesis, which is a critical event during placental growth and fetal development (22). Remarkably, we recently discovered an unusual abundance of arginine (4–6 mmol/L) in porcine allantoic fluid during early gestation when placental growth is most rapid (23,24). Therefore, we hypothesized that increasing L-arginine provision may enhance the reproductive performance of pigs. This hypothesis was tested using dietary supplementation with L-arginine-HCl to gilts between 30 and 114 d of gestation.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Animals and diets. This study was approved by the Texas Tech University Animal Care and Use Committee. A total of 52 gilts (Camborough 22, Pig Improvement) with initial body weight (BW) of 166.3 ± 1.8 kg and backfat (BF) of 13.3 ± 0.2 mm were used in this study. They were housed individually in gestation crates (2.12 x 0.61 m).

All gilts were checked for estrus once daily in the morning and inseminated twice with unfrozen semen via artificial insemination during estrus (18–24 h apart). At d 30 of gestation, gilts were assigned randomly to 1 of the 2 treatment groups representing supplementation with 1% L-arginine-HCl or 1.7% L-alanine (isonitrogenous control) to a corn- and soybean meal-based diet (Table 1). The supplemental level of 1% L-arginine-HCl was chosen because it was shown in our preliminary study to increase plasma concentration of arginine by 70% at 2 h after feeding. L-Arginine-HCl or L-alanine (Ajinomoto) was added to the basal diet at the expense of molasses cane. Alanine was chosen for the isonitrogenous control diet, because it is neither toxic nor a substrate for arginine synthesis but is extensively catabolized by pigs (25,26). There were 28 and 24 gilts in the control and arginine-supplemented groups, respectively. The number of gilts differed between the 2 treatment groups, because some gilts initially allotted to the study were nonpregnant. All gilts received 2 kg diet (on an as-fed basis) daily as 2 equal-sized meals (0700 and 1800) during the entire gestation period. Both diets provided 13.0 MJ metabolizable energy/kg and 12.2% crude protein (on an as-fed basis). Pregnant gilts had free access to drinking water and ate all the feed offered throughout the experiment.


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  		TABLE 1 Composition of gestation diets (on an as-fed basis)1

 
BW and BF thickness were measured on d 30, 70, 90, and 110 of gestation. BF thickness was measured by ultrasound (Keiki LS-1000, Tokimec) at the P2 position (left side of the 10th rib and 6 cm away from the spine). Blood samples were collected at 2 h after feeding via jugular venepuncture into heparinized tubes (Becton-Dickinson Vacutainer Systems) on d 30, 70, 90, and 110 of gestation. Samples were centrifuged at 2000 x g; 15 min at 4°C. Plasma was transferred to 1.5 microcentrifuge tubes (National Scientific) and stored at –20°C until analysis. At d 110 of gestation, all pregnant gilts were transferred to individual farrowing crates (1.5 x 2.2 m). We counted the total number of piglets and recorded their BW at birth. The piglets were further classified as born alive or dead. The piglets born dead referred only to stillborns, which were recorded within 12 h after parturition as any piglets found dead during or shortly after farrowing. These stillborns were mostly fully-formed pigs, which had no characteristics of mummified fetuses, such as dark color, bloated stomach, sunken eyes, loose skin, or bad odor. The piglets found dead under or near the mammary gland were assumed to have died by crushing and were not included as stillborns. An attempt to thoroughly inspect all placentae was made; however, the placentae from 4 gilts fell through the slatted floors and could not be recovered. Among 48 gilts examined, only 3 mummified fetuses were observed. Thus, the number of mummified fetuses (early gestation deaths) was negligible and the number of piglets born dead represented almost entirely fetal deaths during late gestation.

    Chemical analyses. Plasma samples were assayed for urea concentrations using a colorimetric method involving reaction with phenol and hypochlorite, as previously described (27). Plasma concentrations of amino acids were analyzed by HPLC methods involving precolumn derivatization with o-phthaldialdehyde, as described by Wu et al. (27). Amino acid standards and other chemicals were obtained from Sigma Chemical.

    Statistical analysis. Data were analyzed using MIXED procedures of SAS (SAS Institute) following a randomized complete block design. Gilt was considered as the experimental unit. Data for the number of piglets born dead were analyzed using the Friedman test of SAS. Separation of means was performed using the PDIFF option of SAS. P < 0.05 was considered significant. Values in the text are means ± pooled SEM.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Gestation performance. Initial BW or BF thickness of gilts did not differ between the arginine-supplemented and control groups. Similarly, BW and BF did not differ between arginine-supplemented and control gilts throughout the experimental period. The BW of gilts were 166.3 ± 1.8, 183.4 ± 2.3, 193.6 ± 2.9, and 204.6 ± 4.25 kg at d 30, 70, 90, and 110 of gestation, respectively. The BF thickness of gilts was 13.3 ± 0.2, 13.8 ± 0.4, 14.0 ± 0.4, and 15.6 ± 0.3 mm at d 30, 70, 90, and 110 of gestation, respectively. Gestation length (114 ± 0.3 d, n = 52) did not differ between control and arginine-supplemented gilts.

Gilts farrowed during June (25%), July (29%), August (21%), and September (25%) in 2004. The proportion of farrowing that occurred in each of these months did not differ between control and arginine-supplemented gilts. The total number of piglets born did not differ between the 2 groups of gilts (Table 2). However, the total number of piglets born alive was 22% higher (P = 0.032) for arginine-supplemented gilts compared with gilts fed the control diet (Table 2). The average birth weights of all piglets born or of piglets born alive did not differ between the 2 treatment groups. Total litter birth weights, based on the total number of piglets born per litter, did not differ between control and arginine-supplemented gilts; however, total live litter birth weights, based on the total number of piglets born alive per litter, were 24% higher (P = 0.003) for the arginine-supplemented gilts compared with the control group (Table 2). The number of piglets born dead was 65% lower (P = 0.037) for the arginine-supplemented gilts compared with the control group. Variations in birth weights of piglets did not differ between the 2 groups of gilts, whether based on the total number of piglets born or total number of piglets born alive.


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  		TABLE 2 Reproductive performance of gilts fed diets supplemented with or without 1% L-arginine HCl1

 
    Plasma urea concentrations. Concentrations of urea in plasma did not differ between the control and arginine-supplemented groups at d 30 or d 70 of gestation (Table 3). However, concentrations of urea in plasma were 14% and 21% lower in arginine-supplemented gilts than in the control group of gilts at d 90 (P < 0.010) and d 110 (P < 0.001) of gestation, respectively (Table 3).


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  		TABLE 3 Plasma concentrations of urea in gilts fed diets supplemented with or without 1% L-arginine HCl1

 
    Plasma concentrations of amino acids. Plasma concentrations of all amino acids were not different for the 2 treatment groups of gilts at the start of the study (d 30 of gestation; Table 4). However, at d 70 of gestation, plasma concentrations of proline, ornithine, and arginine were 31% (P < 0.001), 44% (P < 0.001), and 79% (P < 0.001) higher, respectively, in the arginine-supplemented gilts compared with the control group. Plasma concentrations of glutamine were 13% (P = 0.019) lower in arginine-supplemented gilts compared with the control group at d 70 of gestation. Similar results were obtained at d 90 of gestation. At d 110 of gestation, concentrations of proline, ornithine, and arginine in the plasma of arginine-supplemented gilts increased by 29% (P = 0.001), 52% (P = 0.002), and 77% (P < 0.001), respectively, compared with gilts fed the control diet (Table 4). Notably, at d 110 of gestation, concentrations of glutamine in the plasma of arginine-supplemented gilts were 26% lower (P = 0.028) in comparison with the control group. At d 70 and d 110 of gestation, concentrations of alanine in the plasma of the control (alanine-supplemented) gilts were 91 and 35% higher (P < 0.05), respectively, than in arginine-supplemented gilts. At all selected days of gestation, plasma concentrations of other amino acids were not different between the 2 treatment groups of gilts (Table 4).


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  		TABLE 4 Concentrations of amino acids in the plasma of pregnant gilts fed diets supplemented with or without L-arginine HCl1

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Embryonic and fetal losses due to unfavorable intrauterine conditions during gestation represent a major obstacle in maximizing the reproductive efficiency of breeding animals (1,28). As a major factor in influencing the intrauterine environment, maternal nutrition plays an important role in regulating fetal growth, development, and survival (22). Thus, providing the pregnant dam with proper nutrition, including adequate amounts of amino acids, is vital for the growing fetus (4,29,30). Arginine is not only required for protein synthesis and ammonia detoxification but is also a precursor of many metabolically important molecules, including proline, ornithine, polyamines, and NO (13,14). Additionally, arginine is the most abundant nitrogen carrier in fetal pigs and is 1 of the most abundant amino acids deposited in fetal tissues (31) and in allantoic fluid of the porcine conceptus during early gestation (23), reflecting its importance in the survival, growth, and development of fetal pigs. Furthermore, amino acid malnutrition in gestating sows results in lower concentrations of arginine in the placenta and fetal plasma (24), as well as reduced activities of placental NO synthase and ornithine decarboxylase (32). The NO synthase is responsible for the synthesis of NO (the endothelium-derived relaxing factor) from L-arginine, whereas ornithine decarboxylase catalyzes the first and rate-controlling step in the synthesis of polyamines (33). Impaired placental synthesis of both NO and polyamines is considered a major factor contributing to intrauterine growth retardation (1,22). However, it was unknown whether arginine supplementation could improve gestation performance in gilts. An availability of data to address this question will provide the necessary foundation for guiding future studies to define the molecular and cellular mechanisms whereby arginine supplementation enhances placental development as well as fetal survival and growth.

The results from this study demonstrate for the first time, to our knowledge, that arginine supplementation to gestation diets for pregnant gilts improved pregnancy outcome by increasing the total number of live-born piglets and total live litter birth weight without any reduction in the average birth weight of piglets. Plasma concentrations of arginine and its metabolites (ornithine and proline) were also increased in arginine-supplemented gilts between d 70 and d 110 of gestation, which coincides with the period of rapid fetal growth (4). Previous reports have shown that uterine capacity starts to become limiting for embryonic survival at as early as 30 d of gestation, thereby affecting fetal growth (3,34) and leading to losses of viable fetuses. Although the majority of the conceptus loss occurs during the peri-implanation period, there is evidence that significant losses also occur during later gestation (35). This is in agreement with the finding of this study that almost all piglets born dead were fully formed, suggesting that these fetal deaths occurred during late gestation. Dietary arginine supplementation reduced the number of stillborn piglets, probably due to an improved uterine environment for fetal growth and development (1). Importantly, no differences were noted in plasma concentrations of lysine and histidine between the control and arginine-supplemented gilts at d 70 to 110 of gestation (Table 4), indicating a lack of an imbalance among basic amino acids. Although plasma concentrations of alanine were increased in the isonitrogenous control group of gilts due to the addition of alanine to the basal diet, their reproductive performance was similar to that of nonsupplemented pregnant gilts at the Texas Tech Swine Research Farm (6), indicating that alanine had no adverse effect on the performance or metabolism of pregnant gilts. Notably, the gilts in this study farrowed during the 2004 summer (June to September) with high ambient temperatures (35–40°C) in Lubbock, Texas. The relatively high number of stillborns that occurred in the control group was typical of gilts that farrowed in the summer months on the Texas Tech Swine Research Farm. For example, our records indicate that, in recent years (2004–2006), the numbers of total piglets born, total piglets born alive, and total piglets born dead per litter were 11.30 ± 0.28 (ranging from 7 to 17 heads), 9.80 ± 0.37 (ranging from 6 to 16 heads), and 1.58 ± 0.29 (ranging from 0 to 8 heads), respectively (n = 270 gilts). Thus, in this study, heat stress may explain the relatively high mean rate of stillbirths (1.86 per litter) in the control group of gilts. Importantly, dietary supplementation with arginine to gilts between d 30 and 114 of gestation enhances the viability of fetal pigs even under this adverse environmental condition.

It is currently unknown how dietary supplementation with L-arginine increased the number of piglets born alive or live litter birth weight. The arginine treatment may enhance placental angiogenesis and growth during early- to mid-gestation, thereby promoting an optimal intrauterine environment throughout pregnancy (22). Additionally, previous studies showed that uterine uptake of arginine may not be sufficient to meet fetal growth requirements during late gestation in pigs (31). In pregnant gilts, as reported previously for pregnant sheep (36), an increase in plasma concentrations of arginine likely resulted in enhancement of its placental transport from mother to fetus. This would provide adequate amounts of arginine from the pregnant gilt to her fetuses, thereby supporting their optimal metabolism and growth during the period of most rapid fetal growth. Indeed, results of a recent study showed that arginine infusion into ewes during late gestation increased protein accretion in fetal lambs (37).

Arginase activity is virtually absent from the porcine placenta (38). Thus, the conversion of arginine into ornithine and proline via the arginase pathway in other maternal tissues and the subsequent catabolism of proline to yield ornithine in the porcine placenta play an important role in placental synthesis of polyamines (1). In support of this notion, plasma concentrations of both ornithine and proline increased in arginine-supplemented gilts (Table 4). In addition, proline and hydroxyproline (major components of collagen) are the only amino acids that exhibit a progressive increase in fetal pigs between d 40 and 114 of gestation (31). The high concentrations of proline in plasma are closely associated with maximal placental growth at d 60 to 70 of gestation (38). Also, elevated levels of plasma proline were observed in arginine-supplemented gilts at d 70 and 110 of gestation (Table 4), which coincide with the progressive increase in proline concentrations in porcine allantoic fluid between d 60 and 110 of gestation (38). This increase in plasma proline concentration further gives credence to the beneficial effect of arginine supplementation, because the uterine uptake of both proline and hydroxyproline only marginally meets fetal pig growth requirements during late gestation (31). Therefore, it is possible that dietary supplementation with arginine increased the provision of ornithine and proline for the synthesis of NO, polyamines, and collagen in the placenta and fetus, as reported for adult rats (13,39). The outcome would be to enhance placental angiogenesis and growth (including vascular growth), utero-placental blood flow, the transfer of nutrients from mother to fetus, and, therefore, fetal survival, growth, and development (1,22,40).

Finally, the finding that concentrations of glutamine and urea were reduced in the plasma of arginine-supplemented gilts (Tables 3 and 4) deserves comments. Arginine supplementation may reduce whole-body amino acid degradation and, thus, urea production as well as the endogenous synthesis of glutamine from branched-chain amino acids and ammonia. Our finding that live litter size and live litter birth weights increased in arginine-supplemented gilts compared with control gilts despite their same feed intake (Table 2) suggests an improvement in the efficiency of utilization of dietary amino acids for fetal growth. Similarly, dietary supplementation with arginine reduced urea concentrations in the plasma of milk-fed piglets and increased the efficiency of utilization of dietary protein for neonatal growth (25).

In conclusion, dietary supplementation with L-arginine markedly enhanced the reproductive performance of gilts by increasing fetal survival and live litter birth weight. This novel and important finding has important practical implications for enhancing fetal survival and growth in pigs and other mammalian species. Further, our results provide a necessary foundation for future studies to define the mechanisms responsible for the beneficial effect of arginine in improving pregnancy outcome in gilts.


   FOOTNOTES
 
1 Supported by Rural Development Administration (Korea), National Research Initiative Competitive Grants (2001-35203-11247 and 2003-35206-13694) from the U.S. Department of Agriculture-CREES, Texas Agricultural Experiment Station (H-8200), and Ajinomoto Co., Inc. (Japan). Back

6 Abbreviations used: BF, backfat thickness; BW, body weight; NO, nitric oxide. Back

Manuscript received 15 November 2006. Initial review completed 5 December 2006. Revision accepted 26 December 2006.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

1. Wu G, Bazer FW, Wallace JM, Spencer TE. Intrauterine growth retardation: implications for the animal sciences. J Anim Sci. 2006;84:2316–37.[Abstract/Free Full Text]

2. Perry JS, Rowlands IW. Early pregnancy in the pig. J Reprod Fertil. 1962;4:175–88.

3. Pope WF. Embryonic mortality in swine. In: Geisert RD, editor. Embryonic mortality in domestic species. Boca Raton (FL): CRC; 1994. p. 53–78.

4. McPherson RL, Ji F, Wu G, Blanton JR Jr, Kim SW. Growth and compositional changes of fetal tissues in pigs. J Anim Sci. 2004;82:2534–40.[Abstract/Free Full Text]

5. Pond WG, Mersmann HJ. 2001 General characteristics. In: Pond WG, Mersmann HJ, editors. Biology of the domestic pig. Ithaca (NY): Cornell University; 2001. p. 1–40.

6. Kim SW, Wu G, Baker DH. Amino acid nutrition of breeding sows during gestation and lactation. Pigs News Inform. 2005;26:N89–99.

7. Pere MC, Etienne M. Uterine blood flow in sows: effects of pregnancy stage and litter size. Reprod Nutr Dev. 2000;40:369–82.[Medline]

8. Reynolds LP, Ford SP, Ferell CL. Blood flow and steroid and nutrient uptake of the gravid uterus and fetus of sows. J Anim Sci. 1985;61:968–74.[Abstract/Free Full Text]

9. Pere MC, Dourmand JY, Etienne M. Effect of number of pig embryos in the uterus on their survival and development and on maternal metabolism. J Anim Sci. 1997;75:1337–42.[Abstract/Free Full Text]

10. Johnson RK, Nielsen MK, Casey DS. Responses in ovulation rate, embryo survival, and litter traits in swine to 14 generations of selection to increase litter size. J Anim Sci. 1999;77:541–57.[Abstract/Free Full Text]

11. van der Lende T, van Rens BT. Critical periods for foetal mortality in gilts identified by analysing the length distribution of mummified foetuses and frequency of non-fresh stillborn piglets. Anim Reprod Sci. 2003;75:141–50.[Medline]

12. Vallet JL, Leymaster KA, Christenson RK. The influence of uterine function on embryonic and fetal survival. J Anim Sci. 2002;80:E115–25.[Abstract/Free Full Text]

13. Wu G, Morris SM. Arginine metabolism: nitric oxide and beyond. Biochem J. 1998;336:1–17.

14. Kim SW, Mateo RD, Yin Y-L, Wu G. Functional amino acids and fatty acids for enhancing production performance of sows and piglets. Asian-Aust J Anim Sci. 2007;20:295–306.

15. Sladek SM, Magness RR, Conrad KP. Nitric oxide and pregnancy. Am J Physiol Regul Integr Comp Physiol. 1997;272:R441–63.[Abstract/Free Full Text]

16. Gardner DS, Powlson AS, Giussani DA. An in vivo nitric oxide clamp to investigate the influence of nitric oxide on continuous umbilical blood flow during acute hypoxaemia in the sheep fetus. J Physiol. 2001;537:587–96.[Abstract/Free Full Text]

17. Fan WQ, Smolich JJ, Wild J, Yu VYH, Walker AM. Major vasodilator role for nitric oxide in the gastrointestinal circulation of the mid-gestation fetal lamb. Pediatr Res. 1998;44:344–50.[Medline]

18. McCrabb GJ, Harding R. Role of nitric oxide in the regulation of cerebral blood flow in the ovine foetus. Clin Exp Pharmacol Physiol. 1996;23:855–60.[Medline]

19. Fozard JR, Part ML, Prakash NJ, Grove J, Schechter PJ, Sjoerdsma A, Koch-Weser J. L-ornithine decarboxylase: an essential role in early mammalian embryogenesis. Science. 1980;208:505–8.[Abstract/Free Full Text]

20. Hoshiai H, Lin YC, Loring JM, Perelle BA, Villee CA. Ornithine decarboxylase activity and polyamine content of the placenta and decidual tissue in the rat. Placenta. 1981;2:105–16.[Medline]

21. Reynolds LP, Redmer DA. Angiogenesis in the placenta. Biol Reprod. 2001;64:1033–40.[Abstract/Free Full Text]

22. Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. Maternal nutrition and fetal development. J Nutr. 2004;134:2169–72.[Abstract/Free Full Text]

23. Wu G, Bazer FW, Tuo W, Flynn SP. Unusual abundance of arginine and ornithine in porcine allantoic fluid. Biol Reprod. 1996;54:1261–5.[Abstract]

24. Wu G, Pond WG, Ott TL, Bazer FW. Maternal dietary protein deficiency decreases amino acid concentrations in fetal plasma and allantoic fluid of pigs. J Nutr. 1998;128:894–902.[Abstract/Free Full Text]

25. Kim SW, McPherson RL, Wu G. Dietary arginine supplementation enhances the growth of milk fed young pigs. J Nutr. 2004;134:625–30.[Abstract/Free Full Text]

26. Wu G, Knabe DA, Kim SW. Arginine nutrition in neonatal pigs. J Nutr. 2004;134:S2783–90.[Abstract/Free Full Text]

27. Wu G, Knabe DA. Free and protein bound amino acids in sows colostrum and milk. J Nutr. 1994;124:2437–44.[Abstract/Free Full Text]

28. Vonnahme KA, Wilson ME, Ford SP. Role of vascular endothelial growth factor in modulating placental/endometrial vascularity in the pig. Biol Reprod. 2001;64:1821–5.[Abstract/Free Full Text]

29. Snoeck A, Remacle C, Reusens B, Hoet JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancrease. Biol Neonate. 1990;57:107–18.[Medline]

30. Hoet JJ, Hanson MA. Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development. J Physiol. 1999;514:617–27.[Abstract/Free Full Text]

31. Wu G, Ott TL, Knabe DA, Bazer FW. 1999. Amino acid composition of the fetal pig. J Nutr. 1999;129:1031–8.[Abstract/Free Full Text]

32. Wu G, Pond WG, Flynn SP, Ott LT, Bazer FW. Maternal dietary protein deficiency decreases nitric oxide synthase and ornithine decarboxylase activities in placenta and endometrium of pigs during early gestation. J Nutr. 1998;128:2395–402.[Abstract/Free Full Text]

33. Pegg AE. Recent advances in the biochemistry of polyamines in eukaryotes. Biochem J. 1986;234:249–62.[Medline]

34. Christenson RK, Leymaster KA, Young LD. Justification of unilateral hysterectomy-ovariectomy as a model to evaluate uterine capacity in swine. J Anim Sci. 1987;65:738–44.[Abstract/Free Full Text]

35. Wilson ME. 2002. Role of placental function in mediating conceptus growth and survival. J Anim Sci. 2002;80 Suppl 2:E195–201.[Abstract/Free Full Text]

36. Thureen PJ, Baron KA, Fennessey PV, Hay WW Jr. Ovine placental and fetal arginine metabolism at normal and increased maternal plasma arginine concentrations. Pediatr Res. 2002;51:464–71.[Medline]

37. De Boo HA, Van Zijl PJ, Smith DEC, Kulik W, Lafeber HN, Harding JE. Arginine and mixed amino acids increase protein accretion in growth restricted and normal ovine fetus by different mechanisms. Pediatr Res. 2005;58:270–7.[Medline]

38. Wu G, Bazer FW, Hu J, Johnson GA, Spencer TE. Polyamine synthesis from proline in the developing porcine placenta. Biol Reprod. 2005;72:842–50.[Abstract/Free Full Text]

39. Kohli R, Meininger CJ, Haynes TE, Yan W, Self JT, Wu G. Dietary L-arginine supplementation enhances endothelial nitric oxide synthesis in streptozotocin-induced diabetic rats. J Nutr. 2004;134:600–8.[Abstract/Free Full Text]

40. Kwon H, Wu G, Meininger CJ, Bazer FW, Spencer TE. Developmental changes in nitric oxide synthesis in the ovine placenta. Biol Reprod. 2004;70:679–86.[Abstract/Free Full Text]




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