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The Journal of Nutrition Vol. 128 No. 5 May 1998,
pp. 894-902
,
* Department of Animal Science, Texas A&M University, College Station, TX 77843 and USDA/ARS Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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This study was conducted to test the hypothesis that maternal dietary protein deficiency decreases amino acid availability to the fetus, thereby contributing to retarded fetal growth. Primiparous gilts selected genetically for low or high plasma total cholesterol concentrations (low line and high line, respectively) were mated, and then fed 1.8 kg/d of isocaloric diets containing 13% or 0.5% crude protein. At d 40 or 60 of gestation, they were hysterectomized, and maternal and fetal blood samples as well as amniotic and allantoic fluids were obtained for analyses of amino acids, ammonia and urea. Dietary protein restriction decreased (P < 0.05) the following: 1) maternal plasma concentrations of urea at d 40 and 60 of gestation; 2) fetal plasma concentrations of alanine, arginine, branched-chain amino acids (BCAA), glutamine, glycine, lysine, ornithine, proline, taurine, threonine and urea at d 60 of gestation; 3) amniotic and allantoic fluid concentrations of urea at d 40 and 60 of gestation; and 4) allantoic fluid concentrations of alanine, arginine, BCAA, citrulline, cystine, glycine, histidine, methionine, proline, serine, taurine, threonine and tyrosine at d 40 of gestation, in gilts of both genetic lines. At d 60 of gestation, protein deficiency decreased (P < 0.05) allantoic fluid concentrations of arginine, cystine, glycine, taurine and tyrosine in low line gilts and of cystine, glutamine, ornithine, serine, taurine and tyrosine in high line gilts. Low line and high line gilts also differed remarkably in allantoic fluid concentrations of arginine, glutamine, ornithine and ammonia at d 40 and 60 of gestation. Our results suggest the following: 1) protein-deficient gilts maintain maternal plasma concentrations of amino acids by mobilizing maternal protein stores and decreasing oxidation of amino acids during the first half of gestation; 2) protein deficiency may impair placental transport of amino acids from the maternal to the fetal blood; and 3) low line and high line gilts differ in fetal amino acid metabolism. Decreases in concentrations of the essential and nonessential amino acids in the fetus may be a mechanism whereby maternal dietary protein restriction results in fetal growth retardation.
KEY WORDS: protein malnutrition · amino acids · pregnancy · fetus · pigs
Since the pioneering work of Evvard et al. (1914) Amino acids are not only the building blocks of proteins and peptides, but also essential precursors for the synthesis of important molecules such as hormones, neurotransmitters, purine and pyrimidine nucleotides, polyamines, creatine, carnitine, porphyrins (Reeds and Hutchens 1994 Chemicals.
HPLC-grade water and methanol were obtained from Fisher Scientific (Fair Lawn, NJ). All other chemicals used in this study for analysis of amino acids, urea and ammonia were purchased from Sigma Chemical (St. Louis, MO).
Pigs.
This study was approved by Texas A&M University's Institutional Animal Care and Use Committee and by Baylor College of Medicine's Institutional Animal Care and Use Committee. Primiparous gilts selected genetically for low or high plasma total cholesterol concentrations (low line and high line, respectively) (Pond et al. 1997
Collection and processing of fetal and maternal blood, amniotic and allantoic fluids.
All gilts were hysterectomized as described previously (Wu et al. 1995 Statistical analysis.
Data were analyzed by two-way ANOVA with Student-Newman-Keuls multiple range test (Steel and Torrie 1980 Amino acids, ammonia and urea in maternal uterine arterial plasma.
There were no differences (P > 0.05) in maternal uterine arterial plasma concentrations of all amino acids between d 40 and 60 of gestation in low line or high line gilts. Therefore, data were pooled for statistical analysis and are shown in Table 2 and Appendix 1. Except for glutamate in gilts fed the 13% crude protein diet, there were no differences (P > 0.05) in maternal plasma concentrations of the other amino acids between low line and high line gilts. In low line gilts, protein deficiency increased (P < 0.05) plasma concentrations of alanine, aspartate, glutamate and lysine, but had no effect (P > 0.05) on the other amino acids. In high line gilts, protein restriction increased (P < 0.05) plasma concentrations of alanine and lysine, but had no effect (P > 0.05) on the other amino acids. Glycine was the predominant amino acid in maternal plasma of pigs, regardless of dietary protein treatment. Protein deficiency decreased (P < 0.05) maternal plasma concentrations of urea, but had no effect (P > 0.05) on ammonia in either low line or high line gilts.
Amino acids, ammonia and urea in fetal umbilical venous plasma.
Table 3 summarizes amino acid concentrations in fetal umbilical venous plasma at d 60 of gestation. In low line and high line gilts, protein deficiency decreased (P < 0.05) umbilical venous plasma concentrations of alanine, arginine, branched-chain amino acids (BCAA; isoleucine, leucine and valine), cystine, glutamine, glycine, lysine, ornithine, proline, taurine and threonine, but had no effect (P > 0.05) on other amino acids. Protein deficiency decreased (P < 0.05) fetal plasma concentrations of urea, but had no effect (P > 0.05) on ammonia in low line and high line gilts.
Amino acids, ammonia and urea in amniotic fluid.
Concentrations of amino acids, ammonia and urea in amniotic fluid at d 40 of gestation are shown in Table 4 and Appendix 2, and those at d 60 of gestation are presented in Table 5 and Appendix 3. In low line gilts, at d 40 of gestation, protein deficiency increased (P < 0.05) amniotic fluid concentrations of glutamate and serine, decreased (P < 0.05) those of phenylalanine and tyrosine, and had no effect (P > 0.05) on the other amino acids. In high line gilts, protein deficiency increased (P < 0.05) amniotic fluid concentrations of BCAA and glutamate, and had no effect (P > 0.05) on the other amino acids. At d 60 of gestation, protein deficiency decreased (P < 0.05) amniotic fluid concentrations of histidine in low line gilts, and of arginine, histidine and ornithine in high line gilts, but increased (P < 0.05) amniotic fluid concentrations of glycine in high line gilts. In low line gilts, protein deficiency had no effect (P > 0.05) on amniotic fluid concentrations of ammonia at d 40 and 60 of gestation. However, in high line gilts, protein restriction increased amniotic fluid concentrations of ammonia at d 60 of gestation. Glutamine was the most abundant amino acid in amniotic fluid of pigs at d 40 and 60 of gestation, regardless of dietary protein treatment. At d 40 and 60 of gestation, protein restriction decreased (P < 0.05) amniotic fluid concentrations of urea in gilts of both genetic lines.
Amino acids, ammonia and urea in allantoic fluid.
Concentrations of amino acids, ammonia and urea in allantoic fluid on d 40 and 60 of gestation are summarized in Tables 6 and 7, respectively. At d 40 of gestation, protein deficiency increased (P < 0.05) allantoic fluid concentrations of aspartate, decreased (P < 0.05) those of alanine, asparagine, BCAA, citrulline, cystine, glycine, histidine, lysine, methionine, proline, serine, taurine, threonine and tyrosine, but had no effect (P > 0.05) on the other amino acids in gilts of either genetic line. The extent to which allantoic fluid amino acids (except for proline, taurine and tyrosine) decreased (P < 0.05) in response to dietary protein deficiency was greater in low line gilts than in high line gilts. Allantoic fluid concentrations of arginine and ornithine in high line gilts were only ~50% of those in low line gilts at d 40 of gestation, regardless of dietary protein treatment. At d 60 of gestation, protein deficiency decreased (P < 0.05) allantoic fluid concentrations of arginine, cystine, glycine, taurine and tyrosine, but had no effect (P > 0.05) on the other amino acids in low line gilts. In high line gilts at d 60 of gestation, protein deficiency increased (P < 0.05) allantoic fluid concentrations of aspartate, glutamate and glycine, and decreased (P < 0.05) those of cystine, glutamine, ornithine, serine, taurine and tyrosine. Interestingly, at d 60 of gestation, allantoic fluid concentrations of arginine, asparagine, citrulline, glutamine, histidine, lysine, ornithine and threonine were much greater in high line gilts than in low line gilts, regardless of dietary protein treatment. At d 40 and 60 of gestation, arginine, glutamate, glutamine, glycine, lysine and ornithine were abundant amino acids in allantoic fluids of both low line and high line gilts. In low line gilts, protein deficiency decreased (P < 0.05) allantoic fluid concentrations of ammonia at d 60 of gestation, but had no effect (P > 0.05) at d 40 of gestation. In high line gilts, protein deficiency increased (P < 0.05) ammonia concentrations at d 40 of gestation and had no effect at d 60 of gestation. Note that allantoic fluid concentrations of ammonia were four- to fivefold greater in high line gilts than in low line gilts at d 60 of gestation, regardless of dietary protein treatments. In gilts of both genetic lines at d 40 and 60 of gestation, protein deficiency markedly decreased (P < 0.05) allantoic fluid concentrations of urea.
Previous studies have shown that maternal dietary protein deficiency decreases placental size in pigs (Schoknecht et al. 1994
We thank Sean Flynn, Wene Yan and John Nelson for technical assistance.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
demonstrating that maternal dietary protein deficiency resulted in lower birth weights and decreased vigor of the offspring in pigs, there have been extensive studies of the effects of dietary protein restriction on fetal growth in humans, pigs and rats (Atinmo et al. 1974 and 1976, Desai et al. 1996, Jain et al. 1995, Pond 1973, Pond et al. 1968, 1969, 1991 and 1992, Schoknecht et al. 1993 and 1994, Widdowson 1977, Zeman and Stanbrough, 1969). Collectively, these studies have shown that protein deficiency during early or midgestation results in decreased placental and fetal growth and may permanently retard postnatal growth. In pigs, protein deficiency during the first trimester of pregnancy has a greater detrimental effect on fetal development than during late pregnancy (Pond 1973, Pond et al. 1968, 1969, 1991 and 1992), suggesting that during the period of embryo implantation (e.g., d 13-30 of gestation in pigs) and placental development, fetal growth is most vulnerable to maternal protein deficiency. Protein malnutrition during pregnancy leads not only to decreased growth of organs but also to permanent alterations in their structure, metabolism and function (Desai et al. 1996, Ozanne et al. 1997, Schoknecht et al. 1993, Widdowson 1977). These findings have important implications for postnatal health, because recent epidemiological studies suggest that in humans there are links between impaired growth during early prenatal life and development of chronic diseases such as diabetes, hypertension and coronary heart disease much later in life (Barker et al. 1990 and 1993, Stein et al. 1996). Although maternal and fetal serum concentrations of insulin-like growth factor (IGF)-I and IGF-II, as well as maternal serum concentrations of placental lactogen, were reported to decrease in protein-deficient pregnant rats (Pilistine et al. 1984), the mechanism for impaired fetal growth in protein-deficient dams remains largely unknown.
) and nitric oxide (NO) (Moncada and Higgs 1993). Polyamines, synthesized from ornithine (ultimately arginine) by ornithine decarboxylase, are essential to early mammalian embryogenesis (Fozard et al. 1980) and to the proliferation of tissues including the placenta (Williams and McAnulty 1976). In addition, NO, synthesized from arginine by NO synthase, was reported to be essential for fertilization (Herrero et al. 1996), embryo attachment and development in the uterus (Norman 1996, Novaro et al. 1997), and plays a critical role in regulating uterine blood flow and thus nutrient supply to the fetus during gestation (Sladek et al. 1997). In addition, amino acids are an important source of energy for the growing fetus (Bell et al. 1989) as well as regulators of embryo development and viability (Lane and Gardner 1997, Petters et al. 1990). Furthermore, glutamine plays a major role in fetal nitrogen and carbon metabolism (Vaughn et al. 1995). The vital roles of amino acids in fetal nutrition and metabolism are consistent with our recent findings of the predominance of glutamine in fetal plasma and amniotic fluid of pigs, and the unusual abundance of arginine and ornithine in the allantoic fluid of pigs (Wu et al. 1995 and 1996). However, there is limited information on the effect of protein deficiency on maternal or fetal plasma concentrations of amino acids during pregnancy. Also, there is no report of the effect of maternal protein deficiency on amino acid concentrations in fetal amniotic or allantoic fluid. We hypothesized that dietary protein deficiency may result in decreased amino acid availability to the fetus, thereby contributing, in part, to impaired placental and fetal growth and development. This hypothesis was tested in this study with use of gilts fed a protein-restricted diet for the first 40 or 60 d of gestation. Days 40 and 60 of pregnancy were selected for sample collections on the basis of previous findings as follows: 1) events in early gestation (e.g., d 40) are critical to porcine fetal growth and development (Bazer 1989, Pond and Maner 1984); 2) placental development is maximal by d 60 of gestation (Knight et al. 1977); 3) placental and fetal growth retardation in maternal protein deficiency are manifested by d 60 of gestation (Pond et al. 1992, Schoknecht et al. 1994); and 4) allantoic fluid arginine, ornithine and glutamine are most abundant at d 40 and 60 of gestation (Wu et al. 1995 and 1996).
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
) were housed at the Swine Center of Sam Houston State University. Before mating, gilts were fed a control diet containing 13% crude protein (Table 1). On the day of mating (d 0 of gestation), gilts within each genetic line were assigned randomly to the control or protein-deficient diet (Table 1) and to the 40- or 60-d pregnancy group in a 2 × 2 factorial design (n = 2-3 gilts per cell). Throughout gestation, control and protein-deficient gilts had free access to water and were fed once daily 1.8 kg diet containing 13 and 0.5% crude protein, respectively. Gilts were hysterectomized at d 40 or 60 of gestation. Twenty hours before hysterectomy, gilts were transported from Sam Houston State University to Texas A&M University (College Station, TX) where sample collections were performed as described below, between 0830 and 0900 h, 24 h after the last feeding.
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Table 1.
Diet composition1
). Briefly, pigs were injected intramuscularly with Telazol (2.2 mg/kg body weight) to induce anesthesia, which was maintained with halothane (1-5%). A midventral laparotomy was performed and the reproductive tract was exposed. Maternal uterine arterial blood (3 mL) and fetal umbilical venous blood (1 mL) were collected into heparinized tubes. Blood could not be obtained from the fetal umbilical vein at d 40 of gestation because of the small size of the vessel. Amniotic and allantoic fluids (3 mL) were obtained through the amniochorion and chorio-allantoic membranes, respectively. Blood was centrifuged at 3000 × g, 4°C, for 10 min to obtain plasma. Plasma, amniotic and allantoic samples (1 mL) were deproteinized with 1 mL of 1.5 mol/L HClO4 and neutralized with 0.5 mL of 2 mol/L K2CO3. Analyses of amino acids, ammonia and urea were performed by HPLC and a colorimetric method, respectively, as described previously (Wu and Knabe 1994, Wu et al. 1994). The coefficients of variation for amino acids in maternal and fetal plasma as well as in amniotic and allantoic fluids were <10% among fetuses within a gilt.
). Probability values <0.05 were taken to indicate statistical significance.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
Table 2.
Dietary protein deficiency affected concentrations of some amino acids and urea in maternal uterine arterial plasma of gilts at d 40 and 60 of gestation1
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Table 3.
Concentrations of amino acids, ammonia and urea in fetal umbilical vein plasma of gilts at d 60 of gestation1
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Table 4.
Dietary protein deficiency affected concentrations of some amino acids and urea in amniotic fluid
of fetal pigs at d 40 of gestation1
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Table 5.
Dietary protein deficiency affected concentrations of some amino acids, ammonia and urea in amniotic fluid
of fetal pigs at d 60 of gestation1
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Table 6.
Concentrations of amino acids, ammonia and urea in allantoic fluid of pigs at d 40 of gestation1
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Table 7.
Concentrations of amino acids, ammonia and urea in allantoic fluid of pigs at d 60 of gestation1
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
) and rats (Pilistine et al. 1984), maternal plasma concentrations of protein and albumin in pigs (Pond 1973, Pond et al. 1992) and humans (Jain et al. 1995), and maternal and fetal serum concentrations of IGF-I and IGF-II in rats (Pilistine et al. 1984). Concentrations of several proteins in allantoic fluid also decrease in protein-deficient pigs at d 60 of gestation (Schoknecht et al. 1994). There is limited information on the effect of protein deficiency on maternal or fetal plasma concentrations of amino acids during pregnancy. Malandro et al. (1996) reported that dietary protein deficiency in rats had no effect on maternal serum concentrations of measured amino acids but decreased fetal serum concentrations of some amino acids (no data on arginine, ornithine and citrulline) at d 20 of gestation. These authors suggested that maternal dietary protein deficiency resulted in down-regulation of placental specific amino acid transport proteins (Malandro et al. 1996). We are not aware of published studies on the effect of maternal protein deficiency on amino acid concentrations in fetal amniotic or allantoic fluids.
, Norman 1996, Novaro et al. 1997, Sladek et al. 1997), it is important to determine changes in amino acid concentrations in fetal fluids in protein-restricted gilts to more completely understand the mechanism for intrauterine fetal growth retardation. Genetically divergent pigs selected for low or high plasma total cholesterol concentrations were used in this study to test our hypothesis that dietary protein deficiency may decrease amino acid availability to the fetus. These pigs were established as low and high cholesterol lines by generations of selection for 56-d blood cholesterol concentrations (Pond et al. 1997). Previous studies have shown that litter size (number of fully formed pigs born per litter) and ovulation rate (number of corpora lutea at d 60 of pregnancy) are significantly decreased in gilts of the high cholesterol line compared with gilts of the low cholesterol line (Wise et al. 1993). Thus it was considered of importance to determine whether the reduced reproductive function in high line gilts may be associated with altered patterns of amino acids and their metabolites in maternal plasma and fetal fluids. The 0.5% crude protein diet was chosen because it had previously been shown to induce maternal and fetal protein deficiency on the basis of decreases in plasma protein and urea concentrations as well as in placental and fetal growth (Atinmo et al. 1976, Pond 1973, Pond et al. 1968, 1969, 1991 and 1992, Schoknecht et al. 1994).
), and because our preliminary studies showed that oxidation of BCAA, arginine, glutamine and proline actually decreased in the isolated placenta of protein-deficient gilts compared with control gilts (Wu, G., unpublished data), our results suggest that maternal dietary protein deficiency may impair placental amino acid transport in pregnant pigs. This is consistent with recent findings that dietary protein deficiency decreases the activities of Na+-dependent neutral amino acid transport by placental system A and of cationic amino acid transport by placental system y+ (for basic amino acids) in pregnant rats (Malandro et al. 1996, Varma and Ramakrishnan 1991). Because BCAA, lysine and threonine are not synthesized by mammalian cells, a deficiency of these essential amino acids in fetal blood may contribute to decreases in fetal tissue protein synthesis and in the endogenous synthesis of glutamine and alanine from BCAA by fetal skeletal muscle. Furthermore, the decreased arginine concentration in fetal umbilical vein plasma may result in decreased NO synthesis and therefore reduced blood flow and nutrient supply to the fetus.
). Amniotic fluid is removed through the same channels by both the fetus and the mother, in addition to absorption by the fetal intestine (Schmidt 1992). An interesting finding from this study is that concentrations of amino acids in amniotic fluid did not differ remarkably between control and protein-deficient gilts (Tables 4 and 5, Appendices 2 and 3) at d 40 and 60 of gestation, even though dietary amino acid ingestion by protein-restricted gilts was negligible (Table 1). Our results suggest that the fetus has a mechanism for sparing amniotic fluid amino acids during maternal dietary protein deficiency, which may involve decreased amino acid oxidation. At d 60 of gestation, protein deficiency decreased amniotic fluid concentrations of arginine and ornithine by 37 and 48%, respectively, in high line gilts (Table 5), which may have resulted from decreased entry of arginine and ornithine from the maternal and fetal blood and/or decreased endogenous synthesis of these two amino acids in the fetus. Interestingly, at d 60 of gestation, when the fetal pig liver has developed activities of all urea cycle enzymes (Kennan and Cohen 1959), a deficiency of amniotic fluid arginine and ornithine is associated with a 100% increase in amniotic fluid concentration of ammonia in high line gilts (Table 6). Our results suggest that a deficiency of arginine and ornithine in amniotic fluid may impair fetal ammonia detoxification and that these two amino acids play an important role in fetal nutrition and metabolism.
). The allantoic sac was traditionally considered to be the reservoir of fetal wastes, but later studies have suggested that allantoic fluid is a reservoir of nutrients in the fetus (Bazer 1989). Because nutrients in allantoic fluid can be absorbed by the allantoic epithelium into the fetal-placental circulation (Bazer 1989), the allantoic sac may play an important role in fetal nutrition and metabolism, as originally proposed for iron (Buhi et al. 1983). An important characteristic of allantoic fluid is an unusual abundance of arginine and ornithine at d 40 and 60 of gestation in pigs (Wu et al. 1995 and 1996) (Tables 6 and 7). A novel finding from this study is that, in contrast to amniotic fluid, maternal protein deficiency decreased allantoic fluid concentrations of most amino acids (nutritionally essential and nonessential) at d 40 of gestation, in both genetic lines of gilts (Table 6). These include neutral amino acids (alanine, BCAA, citrulline, cystine, glycine, methionine, proline, serine, taurine, threonine and tyrosine) in low line and high line gilts and some basic amino acids (histidine and lysine) in low line gilts (Table 6). Interestingly, the decreases in allantoic fluid concentrations of amino acids (except for proline, taurine and tyrosine) occurred to a much greater extent in low line gilts than in high line gilts (Table 6). Also, allantoic fluid concentrations of arginine and ornithine in high line gilts were only ~50% of those in low line gilts at d 40 of gestation, regardless of dietary protein treatment. With increasing gestational age from 40 to 60 d, allantoic fluid concentrations of glutamine, arginine and ornithine dramatically decreased by 89, 87 and 67%, respectively, in low line gilts, but those of glutamine and arginine decreased by only 55 and 13%, respectively, in high line gilts. Indeed, allantoic fluid concentrations of ornithine actually increased by 74% at d 60 compared with d 40 of gestation in high line gilts (Tables 6 and 7). This resulted in greater concentrations of glutamine, arginine and ornithine in high line gilts at d 60 compared with d 40 of gestation. These findings suggest marked differences in fetal amino acid metabolism between low line and high line gilts, extending the previously reported differences in plasma metabolites (e.g., total cholesterol, HDL-cholesterol, triglycerides or alkaline phosphatase) (Pond et al. 1997) and in reproductive performance (Wise et al. 1993) between low line and high line gilts.
)], the increases (45-700%) and decreases (33-75%) in amniotic fluid concentrations of amino acids at d 60 of gestation are not likely due to an associated increase in amniotic fluid volume, as suggested for alterations in electrolyte concentrations (McCance and Dickerson 1957). In allantoic fluid, concentrations of all amino acids, except for alanine plus cystine plus glycine (in protein-deficient gilts), arginine plus ornithine (in high line gilts), phenylalanine and tryptophan markedly decreased (P < 0.05) at d 60 compared with d 40 of gestation (Tables 6 and 7). This result is similar to the previously reported decrease of allantoic fluid concentrations of amino acids between d 45 and 60 of gestation in gilts (F1 crosses of Yorkshire × Landrace sows and Duroc × Hampshire boars) fed a sorghum- and soybean meal-based diet containing 13.9% crude protein (Wu et al. 1995). Interestingly, allantoic fluid concentrations of arginine did not significantly alter (P > 0.05) between d 60 and d 40 of gestation in high line gilts, in contrast to low line gilts (Tables 6 and 7) and our previous study (Wu et al. 1995). On the basis of the volume of allantoic fluid in pigs [66 and 322 mL at d 40 and 60 of gestation, respectively (Knight et al. 1977)], the decreases in allantoic fluid concentrations of amino acids (e.g., 85-96% for arginine, glutamine, histidine, serine and threonine in low line gilts) at d 60 of gestation cannot be explained solely by an associated increase in allantoic fluid volume. These findings suggest dynamic exchanges between the amniotic or allantoic compartment and the fetus (A'Zary et al. 1973, Wu et al. 1995), which may be altered for glutamine and its related amino acids (alanine, glutamate, arginine, ornithine and citrulline), glycine and amino acids containing hydroxylic (+OH) groups (serine, threonine and tyrosine) in high line gilts and protein-deficient gilts.
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APPENDIX 1Concentrations of amino acids, ammonia, and urea1
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APPENDIX 2Concentrations of amino acids, ammonia, and urea in amniotic fluid of fetal pigs at d 40 of gestation1
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APPENDIX 3Concentrations of amino acids, ammonia, and urea in amniotic fluid of fetal pigs at d 60 of gestation1
ACKNOWLEDGMENTS
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FOOTNOTES |
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Manuscript received 9 September 1997. Initial reviews completed 2 December 1997. Revision accepted 26 January 1998.
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LITERATURE CITED |
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Abstract
Introduction
Methods
Results
Discussion
References
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effect of maternal undernutrition.
J. Embryol. Exp. Morph.
1976;
35:545-559
[Medline]
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