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School of Dietetics and Human Nutrition, McGill University Macdonald Campus, Montreal, QC, Canada H9X 3V9
2To whom correspondence should be addressed. E-mail: kris.koski{at}mcgill.ca.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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12% and 
24% glucose) and gestational age (d 18/19 and 20/21) showed that 2 AF amino acids, methionine and phenylalanine, and 12 AF amino acids were independently modified by diet and gestational age, respectively. Of note were the 364% increase in AF methionine and the constant decline in AF taurine as both gestational age lengthened and fetal weight increased. Multiple regression demonstrated that in addition to methionine, 3 specific AF amino acids, cysteine, lysine, and tyrosine, predicted fetal weight. These results demonstrate that the AF amino acid pool can be modified by the glucose content of the maternal diet and that specific AF amino acids are associated with gestational age and fetal growth.
KEY WORDS: • amino acids • amniotic fluid • glucose
Amniotic fluid (AF)3 is swallowed by the developing fetus (1), and both its volume and composition play important roles in fetal growth and development. AF, which is a dynamically changing nutrient reservoir, is a composite of secretions from maternal plasma, from the placenta, and from the developing fetal urinary, respiratory, and alimentary tracts (2). Within this complex nutrient matrix, AF glucose, which is considered an important regulatory fuel during fetal development, acts to sustain numerous energy-dependent systems, including placental amino acid uptake (3), and promotes and maintains fetal growth (4).
Several studies have investigated the effect of starvation or carbohydrate restriction on amino acid metabolism (5–9), but few have done so during pregnancy (10–13), and far fewer have measured their effect on AF composition (10,14). Food deprivation in late gestation reportedly decreases AF BCAAs, as well as the gluconeogenic amino acids, alanine and glycine (14). In pregnant women, energy restriction lowers AF concentrations of alanine and results in higher concentrations of AF taurine and BCAAs (10). Evidence relating to other dietary-induced changes in amino acid concentrations in AF is lacking.
Our aim was to explore the possibility that the amino acid profile of AF might be related to fetal growth. Previous research in our laboratory showed that if maternal dietary glucose was limiting, there was high perinatal mortality, morbidity, and intrauterine growth retardation (IUGR) proportional to the degree of maternal dietary glucose restriction (15–17). Glucose is considered to be the principal metabolic fuel for the developing fetus in utero (4,16). Increasing amounts of maternal dietary glucose are associated not only with fetal growth in a dose-dependent manner but also with increasing tissue glycogen reserves and the emergence of important regulatory enzymes associated with perinatal glycogenolysis and gluconeogenesis (18–20). Thus, the possibility existed that this diet-induced model employing restriction of maternal dietary glucose to produce fetal growth retardation could be used to ascertain those AF amino acids specifically related to optimal fetal growth and gestational age and those specific AF amino acids that might be associated with poor maternal dietary glucose intake and predictive of IUGR.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The rationale for the use of these 3 low-carbohydrate diets was based on our earlier observations reporting a change in AF glucose as maternal dietary glucose varied that was proportional to birthweight (4). Additionally, maternal glucose restriction resulted in an increase in AF uric acid that was negatively associated with maternal dietary glucose, which was positively correlated with maternal and fetal liver glycogen and in utero growth (4). Thus, these results strongly suggested that this maternal dietary glucose restriction could also modify AF amino acid concentrations; use of this dietary model could provide insight into the contribution of individual AF amino acids to fetal growth.
Amniotic fluid collection and biochemical analysis. Fetuses were delivered from dams by caesarean section on d 18, 19, 20, or 21 of gestation between 0730 and 1230 h. All dams were killed in the postabsorptive (fed) state under anesthesia with Ketamine-HCl (30 mg/kg, Rogarsetic, Rogar/STB). Immediately after cardiac puncture, intact uteri were removed and an aliquot of AF was collected from each individual sac and pooled by litter. Fetuses were weighed individually and then killed by exsanguination. All procedures were conducted in conformance with the guidelines for experimental procedures set forth by the local animal care committee of McGill University and by the Canadian Council on Animal Care (22). The pooled AF was stored at –80°C until the day before analysis. Immediately after thawing, samples were deproteinized by ultracentrifugation (1500 x g for 30 min) using 10,000 mol/L Millipore cutoff membranes. The concentrations of 18 amino acids in AF (alanine, arginine, aspartic acid, cysteine, glutamic acid, glutamine, glycine, isoleucine, leucine, lysine, methionine, phenylalanine, proline, serine, taurine, threonine, tyrosine, and valine) were measured by HPLC Aminotag, using norleucine as an internal standard. Samples were precolumn derivatized by 9-fluorenylmethyloxychloroformate (FMOC), which was selected for its ability to derivatize low picomolar amounts of amino acids under fluorescence and to produce stable derivatives of both primary and secondary amino acids (23–25). FMOC also surpasses other derivatization methods that have a lengthy analysis time (ninhydrin), produce unstable derivatives (dansyl chlorides), are not able to detect secondary amino acids (o-phthalaldehyde), or whose samples have to be evaporated before analysis (phenylisothiocyanate) (23). Moreover, FMOC derivatization is less sensitive to interference from extraneous sample components in comparison with other methods, and can derivatize amino acids in <1 min (23). Our samples were derivatized immediately before injection into the HPLC to avoid having to extract excess FMOC with amantadine (23).
Statistical analysis.
All statistical analyses were performed using SAS, version 8.0 (26). Amino acid concentrations were analyzed for AF pooled by litter. In addition to individual amino acids, amino acid concentrations were also categorized into essential, nonessential, and conditionally essential groups based on guidelines set by Domenech et al. (27) in which all essential amino acids were considered the same for growing rats as for humans, with the addition of arginine, asparagine, glutamic acid, proline, and tyrosine for rats. The concentration of total free amino acids was also calculated for analysis. The amino acids of glutamic acid and glutamine were combined because interconversion between the 2 is common (28). Concentrations of individual and grouped amino acids were categorized for diets as 12% glucose and 24% glucose, as well as for gestational age as d 18/19 and d 20/21. AF amino acids were tested using a 2 x 2 interaction ANOVA (diet x gestational age). AF amino acid values were also compared using a 1-way ANOVA across quartiles of fetal weight that included gestational age as a covariate. To determine whether any AF amino acids acted as predictors for fetal weight, a multiple regression was performed with mean fetal weights for each dam as a dependent variable, gestational age as an independent variable, and each amino acid or amino acid group individually introduced into the model. Introduction of individual amino acids or amino acid groups into the model was done because there were noteworthy correlations among many amino acids (29). A P < 0.05 was chosen for significance for all statistical analyses including the Student’s t test and Student-Newman-Keuls post-hoc tests.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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There were no significant interactions between diet and gestational age (2-way interaction ANOVA). Diet was the main effect for only 2 amino acids, methionine and phenylalanine, and concentrations of these amino acids were higher in dams fed 24% glucose (n = 32) than in those fed 12% glucose (n = 41) (Table 1). These values were also associated with a higher fetal weight (3.14 ± 0.17 g vs. 4.07 ± 0.23 g for 12 vs. 24%, respectively). Gestational age was a significant main effect for several individual amino acids: alanine, glutamic acid + glutamine, glycine, isoleucine, leucine, methionine, phenylalanine, proline, serine, taurine, threonine, and valine, as well as for grouped amino acids: essential, nonessential, conditionally essential, and total amino acids (Table 1). With the exception of taurine, all AF amino acids increased with gestational age. It may be expected that because AF volume decreases with increasing gestational age, a dilution effect may be contributing to the reported increase in concentration of amino acids as pregnancy progressed; however, there was no constant percentage increase across all amino acids.
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3.30 g) and highest when birthweight was >4.21 g. Taurine declined steadily as term fetal weight increased, with a peak concentration at the lowest quartile (<2.65 g) and a nadir at the highest quartile weights (>4.21 g), whereas threonine had a peak in concentration between 3.3 to 4.21 g (Table 2).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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During starvation, in addition to increased gluconeogenesis, the placenta decreases its high consumption of glucose (36) without changing in size (17) to decrease its demand on maternal glucose and to promote diversion of some maternal glucose from the placenta to the fetus (36). This occurs without alteration in the expression and activity of placental glucose transporters in IUGR fetuses (37). However, this inhibition of glycolysis and aerobic metabolism was shown to suppress amino acid transport across the placenta (38–40), particularly essential amino acids in growth-retarded infants (41) via a reduced activity/expression of amino acid placental transport systems (37). Our data supported this observation for 2 amino acids because AF concentrations of methionine and phenylalanine were lower in glucose-deprived rat dams. Our data did not support the suggestion (42) that the placenta, in times of nutritional deprivation, would supply amino acids to meet fetal needs and regulate fetal growth (37).
Methionine’s importance in growth is demonstrated by its vital role in the production of cysteine and in facilitating DNA and tRNA methylation (43,44). Due to the lack of cystathionase in the fetal human liver and brain, both cysteine and methionine are essential to the fetus and conserved for protein synthesis during rapid growth (43). This conservation is demonstrated in human pregnancies at 8–12 wk gestation; at that time point, methionine was reported to be 4 times higher in the extra-embryonic coelomic fluid and 2 times higher in the AF vs. maternal serum (44). In our study, AF methionine concentrations had the most notable increase, rising 87% when maternal glucose intake increased from 12 to 24%. On the other hand, the concentration of AF methionine increased 364%, from 45 ± 16 µmol/L at a fetal weight < 2.65 g to 209 µmol/L with mean fetal weights > 4.21 g. Additionally, methionine as well as cysteine had high ß-coefficients when associated with fetal weight in a multiple linear regression model. Thus, methionine’s decidedly lower concentration in AF in our growth-retarded fetuses supports the possibility that its shortage during pregnancy may be detrimental to fetal growth and development; previous reports in rats described disturbed morphogenesis and the development of neural tube defects (44). For cysteine, a high ß-coefficient was associated with a maximum change of 2 µmol/L from d 18–21, which would produce no more than a 124 mg increase in fetal weight. The existence of these low concentrations of AF cysteine is likely due to the absence of cystathionase in the fetal brain and liver or to slow placental transfer of cysteine to protect the fetus from toxic cysteine metabolites (43).
Starvation markedly increases plasma BCAA concentrations (10), whereas hyperglycemia decreases all maternal and fetal plasma amino acids by >50%, especially fetal BCAAs, and essential amino acids (35). BCAAs have regularly been associated with protein synthesis, growth and tissue repair (45), and pancreatic development (46). BCAAs are of particular interest in fetal growth because they may be transported to the fetus preferentially (47), rapidly crossing the placenta (48). Others have suggested the existence of nonmaternal sources such as the yolk sac as an important precursor pool (49). Our study reported that concentrations of AF BCAAs were unaltered by maternal glucose intake if gestational age was controlled for in the model and strongly suggested that limiting only maternal dietary glucose was not sufficient to perturb AF BCAA concentrations. BCAAs in our study were associated with gestational age. Because of these results, it is likely that these amino acids were not the regulators of sustained fetal gluconeogenesis when glucose was limiting, as was suggested (36). In agreement with our results, Jozwik et al. (47) reported that fetal plasma glucose levels were not changed after an infusion of BCAAs. This suggests that the fetal utilization of BCAAs is independent of changes in maternal plasma glucose concentrations (47).
In humans, concentrations of several AF amino acids, including BCAAs, alanine, and lysine, reportedly decrease toward the end of pregnancy (29,50,51); however, small increases in AF methionine, phenylalanine, taurine, and tyrosine were also reported (10,52) in rat AF, with the exception of a decreasing trend for taurine (52), which was also observed in the present study. Changes in AF amino acid concentrations as gestational age progressed were most likely regulated by tissue growth, protein deposition, and fetal energy demands, which are developmentally regulated (13). Other variations in AF concentrations during development may also be attributed to factors such as fetal skin keratinization, maturation of renal functions (27), and fetal swallowing (1). It is believed that mothers retain essential and nonessential amino acids equally, whereas the fetus retains more essential amino acids (28,53). Amino acids that are generally retained by the fetal tissues are aspartic acid, cysteine, methionine, lysine, phenylalanine, serine, and threonine (53); therefore, it was not surprising to find that these AF concentrations changed as development progressed in our study. Those that were released by fetal tissues are arginine, glutamic acid, glutamine, and proline (53), and in our study, all of these were correlated with changes in gestational age.
AF taurine differed notably from all other amino acids because it was negatively associated with birthweight. As a multifunctional amino acid, it was not surprising that our study reported levels of AF taurine that varied with fetal weight, although the tendency to differ repeatedly from other amino acid trends was intriguing. As a predominant intracellular free amino acid (54) and a potent antioxidant (55), taurine reportedly plays a role in retinal development and rat glial cell function (56). It also serves as an important organic osmolyte in the brain and kidney, contributing to cell volume regulation (57). It may also play this role for AF volume near term as both declined. Throughout gestation, taurine is present in the human fetal brain, liver, retina, plasma, and placenta in higher amounts than in the respective adult tissues (43), and it is found in high concentration (68 µmol/L) in the AF of infants born appropriate for gestational age (53). However, its specific role in fetal growth is open to interpretation and speculation. We suggest that the higher concentrations of AF taurine that were associated with the lower fetal weights in our study could point to its lower utilization by the relatively immature pups given its involvement in several growth processes.
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FOOTNOTES |
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3 Abbreviations used: AF, amniotic fluid; FMOC, 9-fluorenylmethyloxychloroformate; IUGR, intrauterine growth retardation.
Manuscript received 15 January 2005. Initial review completed 16 March 2005. Revision accepted 31 May 2005.
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