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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:1754-1758, July 2004

Human Nutrition and Metabolism

Total Protein Concentration in Human Amniotic Fluid Is Negatively Associated with Infant Birth Weight1

Daniel K. Tisi, Jessica J. Emard and Kristine G. Koski2

School of Dietetics and Human Nutrition, McGill University (Macdonald Campus), Montréal, Canada H9X-3V9

2To whom correspondence should be addressed. E-mail: kristine.koski{at}mcgill.ca.


   ABSTRACT
TOP
 ABSTRACT
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Our objectives were 2-fold: 1) to assess the concentration and distribution of total protein in human amniotic fluid (AF) using 3 standard assays [Bradford, bicinchoninic acid solution (BCA), and Lowry] and 2) to establish whether these total protein concentrations were associated with and predictive of infant birth weight. Birth outcomes were determined using recently developed birth-weight-for-gestational-age categories (percentiles) for fetal growth where infants < 10% were classified as SGA (small-for-gestational-age), those between 10 and 90% as appropriate-for-gestational-age (AGA) and those infants ≥ 90% as large-for-gestational-age (LGA). AF samples were collected from women undergoing routine amniocentesis for genetic testing (mean = 15 ± 0.04 wk, range 12–20 wk), frozen, and later analyzed for total protein in 617 singleton-expectant mothers in Montréal, QC, Canada. Maternal and fetal characteristics were obtained from questionnaires and medical chart review. Mothers giving birth to LGA infants had uniformly lower AF protein concentrations at 12–20 wk gestation compared with AF protein concentrations for mothers of AGA infants. Multiple regression analyses demonstrated that total AF protein, collected during routine amniocentesis and later analyzed by the Lowry method, was negatively associated with birth weight at term in our population. These data suggest that one or more AF proteins might emerge as biomarkers of fetal growth.

KEY WORDS: • amniotic fluid • total protein • fetal growth • birth weight • Lowry assay

Amniotic fluid (AF)3 is crucial to fetal health because it forms a protective sac around the infant that prevents mechanical and thermal shock, possesses antimicrobial activity, assists in acid/base balance, and contains nutritional factors (1–3). A wide range of proteins has been identified in human AF (4–6). These proteins can enter the amniotic fluid from the maternal uterine tissues, umbilical cord, amniotic fluid cells, fetal urine, meconium, and other fetal secretions that include transudation through fetal skin (4,7,8). AF proteins are principally of maternal origin, have concentrations lower than in maternal serum (9), and reportedly vary between 0.2 and 7 g/L (3,8,10,11). There is also a dynamic temporal pattern, with AF total protein concentrations rising from 7 to 20 wk gestation and declining thereafter (3,4,12).

Fetal swallowing represents the principal mechanism of clearance of AF protein, which is thought to have a half-life of 1–2 d in monkeys (13); however, before keratinization of fetal skin at 24 wk (14), diffusion of the lower-molecular-weight proteins across unkeratinized fetal skin may occur (15). Fetal swallowing of amniotic fluid begins early in development (16), where it was shown that protein can be absorbed from amniotic fluid by the developing fetuses of monkeys and rats (13,17); there is also evidence in monkeys of progressive intestinal proteolysis for 7 d after infusion of radiolabeled protein into AF (13). The absence of fetal swallowing, which accounts for up to 80% of AF protein clearance in late gestation (18), was associated with fetal growth retardation in both animals (19) and humans (16), indicating its importance as a nutrient source during in utero development. Moreover, it was also shown that both transamniotic fluid infusions of bovine amniotic fluid (20) and intragastric infusions after esophageal ligation (21) resulted in augmentation of fetal growth and birth weight.

Correlations between total AF protein content and abnormal fetal development have been reported. Higher concentrations of some key proteins were associated as a biomarker with negative fetal outcomes (4,5,22,23) including insulin-like growth factor binding protein-1 (IGF-BP1) (24) and erythropoietin (EPO) (25,26), prealbumin (27), and abnormal albumin bands (28). However, a negative relation between fetal growth and high maternal serum concentrations of {alpha}-fetoprotein (29) did not occur when AF {alpha}-fetoprotein was measured at the time of routine amniocentesis (30). In contrast, little is known about the relation between amniotic fluid proteins as nutritional status indicators of normal fetal growth. Albumin, transferrin, and ferritin constitute the major proteins found in AF (31). Some studies suggested that cord blood {alpha}-fetoprotein may (32) and may not be (30), cord blood prealbumin may (33,34), and total AF protein (4,7) may be related to fetal growth. However, no relation between amniotic fluid protein absorption and fetal body weight was demonstrated clinically (18,35,36). Because these conclusions were limited by small sample sizes and the failure to control for established predictors of fetal growth and infant birth weight such as gestational age, infant gender, maternal height and prepregnancy weight, smoking, parity, and ethnicity (37), there remains the possibility of an association between total AF proteins or some fraction thereof and fetal growth and development.

Our study objectives were 2-fold: 1) to assess the concentration and distribution of total protein in human AF early in gestation using 3 standard assays [Bradford, bicinchoninic acid solution (BCA), and Lowry] (38) and 2) to establish whether these early AF total protein concentrations were associated with and predictive of infant birth weight. We investigated this relation in a large population of pregnant women (n = 617) undergoing routine amniocentesis for genetic testing in Montréal, Canada. We classified birth weight using the recently developed fetal growth percentiles that define small-for-gestational-age (SGA) as <10% and large-for-gestational-age (LGA) as >90% based on gestational age and gender (39). We hypothesized not only that the concentration of protein in amniotic fluid early in pregnancy might be related to in utero fetal growth and associated with final birth weight, but also that the sensitivity of the particular assay procedures for total protein might vary in amniotic fluid due to the many classes of serum proteins found in amniotic fluid and the wide range of free amino acids that could interfere when classic detection methods for total proteins were applied to this particular biological fluid (4,7).


   SUBJECTS AND METHODS
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 ABSTRACT
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Recruitment. From 2000 to 2002, pregnant women undergoing routine amniocentesis at St Mary’s Hospital Center in Montréal, Canada were invited to participate in this study. Signed consents allowed researchers to obtain AF from Montréal Children’s Hospital once genetic testing was completed. Application of inclusion criteria (singleton pregnancy) and exclusion criteria (multiple births, genetic anomalies) resulted in 617 participants whose AF samples were analyzed and 437 mother-infant pairs for whom birth weights were recorded in the maternal obstetrics chart at the time of delivery. McGill’s Faculty of Medicine’s Institutional Review Board and ethics committees for each of the affiliated hospitals approved all procedures.

    Maternal and fetal characteristics. Maternal and infant characteristics were obtained from questionnaires and maternal medical chart review; access to pediatric charts is granted only if permission is obtained from the provincial government, which was not requested in this study. Self-reported height, prepregnancy weight, age, smoking status (smoking, quit during pregnancy, or never smoked), amniocentesis week, and parity were collected from questionnaires, maternal age, parity, and infant gender; birth weight and gestational age were verified from obstetrical medical chart review. Gestational age was uniformly calculated on the basis of physicians’ estimates using last menstrual period. Ethnicity was classified according to literature describing differing pregnancy characteristics by ethnicity (40–44) and the following groups were created: Caucasian (North American and European), Asian, and other that included Caribbean and African Blacks (8%), Hispanics of Mexican, Central and South American descent (4%) and those of Middle-Eastern decent (6%). BMI was categorized into 4 groups using NIH criteria (45).

    Biochemical analysis. Frozen AF samples were analyzed for total protein in duplicate or triplicate using the Bradford, BCA, and Lowry microassay procedures. All reagents were purchased from Sigma Aldrich, and 96-well protocols were followed according to the manufacturer’s instructions, with the exception of the Lowry assay, in which AF volumes were further diluted by a factor of 10 to analyze the AF samples using 96-well plates. Bovine serum albumin was used as the standard and a 0.85 g/L solution of sodium chloride as the blank. The KC4 Kineticalc Version 2.6, Rev. 3 from Bio-Tek Instruments was used to measure absorbance for all assays at 590 nm.

    Statistical analysis. All data were analyzed using SAS (Version 8.02, SAS Institute). All nonnormally distributed data were log10 transformed. Birth weight was divided into 3 percentile categories using recently developed fetal growth grids that correct for gender and gestational age. Percentile subcategories were SGA (<10%), appropriate-for-gestational age (AGA; 10–90%), and LGA (>90%) (39). A Bland and Altman plot was used to test for bias (46). ANOVA followed by Scheffé multiple comparison tests was performed to determine whether the total protein concentration differed among these birth-weight-for-gestational-age categories and for several maternal characteristics (BMI, ethnicity, and amniocentesis week). After controlling for prepregnancy weight and height, ANCOVA were used to compare total protein concentrations among small (SGA), normal (AGA), or large (LGA) birth-weight-for-gestational-age infants where gestational age and gender were accounted for by the classification system. Multiple regressions for birth weight and birth-weight-for-gestational-age in the whole population were examined with the results for each AF protein assay entered individually and analyzed in separate regression models; in all cases, the 5 well-documented determinants of birth weight (height, prepregnancy weight, smoking status, gestational age, and infant gender) were included (37). Significance was established as P < 0.05.


   RESULTS
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 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
The maternal lifestyle characteristics questionnaire revealed that our population consisted of health-conscious women (>30 y old); 85% were nonsmokers, 98% did not drink either alcohol or caffeinated beverages, and 73% took multivitamin and mineral supplements.

Maternal and amniotic fluid characteristics (n = 617) and infant characteristics (n = 437) are summarized in Table 1. Among our 617 healthy older women undergoing routine amniocentesis for genetic testing, the majority (65%) had prepregnancy weight and BMI within the normal range. The birth weight of the infants was 3394 ± 26 g. AF total protein concentrations, averaged over all gestational ages (amniocentesis wk 12–20), ranged from 0.16–10.0 g/L for the 3 methods. Birth outcomes showed that 84% of infants were in a healthy weight range (2500–3999 g) at birth with only 4% intrauterine growth retarded and 12% macrosomic (>4000 g). Interestingly, with the newer birth-weight-for-gestational-age (percentile ranking), there were more SGA (9%) and fewer AGA (80%), but a similar incidence of LGA (12%).


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  		TABLE 1 Characteristics of the sample population1

 
Pearson correlations among the biochemical measurements for total AF protein were positive for all combinations: Bradford and BCA (r = 0.97, P < 0.01), BCA and Lowry (r = 0.72, P < 0.01), and Bradford and Lowry (r = 0.73, P < 0.01). The Bland and Altman plot revealed no bias (not shown). Moreover, all were normally distributed (Fig. 1) with similar mean concentrations for the BCA and Lowry (3.81 ± 0.1 vs. 3.79 ± 0.1 g/L, respectively) assays, whereas the Bradford assay (3.31 ± 0.1 g/L) was lower. AF protein concentrations did not differ among BMI categories, by ethnicity or by amniocentesis week.



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  		FIGURE 1 Population distribution (n = 617) of amniotic fluid total protein concentration obtained via routine amniocentesis in pregnant women as measured by the Lowry method. Similar results were obtained using the Bradford and BCA methods.

 
Total AF protein concentration measured by the Lowry and BCA methods was lower in the LGA than in the AGA groups with and without the inclusion of the covariates of maternal height and weight and gestational age and infant gender in the statistical analyses (Table 2). For the Bradford assay, inclusion of these covariates resulted in a loss of significance. LGA infants had lower AF total protein concentrations than AGA infants at 15.3 ± 0.04 wk gestation.


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  		TABLE 2 Infant, maternal, and amniotic fluid characteristics stratified by birth weight for gestational age1

 
Multiple regression analysis was performed (Table 3) with all established predictors for birth weight controlled for in both models. Total AF protein measured between 12 and 20 wk gestation was a negative, independent predictor of both birth weight and birth-weight-for-gestational-age in our sample population, but interestingly, only when measured by the Lowry assay. Gestational age was also examined as an outcome variable with maternal height, prepregnancy weight, ethnicity, smoking behavior, amniocentesis week, infant gender, and amniotic fluid total protein concentration obtained between wk 12 and 20 included in the model, but it was predicted only by maternal height and ethnicity (not shown).


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  		TABLE 3 Multiple regressions of birth outcomes by birth weight and gender-corrected-birth-weight-for-gestational-age1

 

   DISCUSSION
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 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Amniotic fluid is a complex protein matrix; although several of its specific proteins have long been associated with the diagnosis of fetal abnormalities (4,7), the extent to which the concentration of total protein in AF might figure in the clinical evaluation of fetal growth has remained largely unexplored. Ours is the first study to investigate this association, and several important results have emerged. Total AF protein concentrations varied widely, ranging from a low of 0.16 to a high of 10.0 g/L early in the 2nd trimester, but our mean concentrations compared favorably with previous studies that had reported AF protein concentration during the 2nd trimester using much smaller sample sizes (8,12,47). We also showed that these protein concentrations did not vary by amniocentesis week, prepregnancy weight, or ethnicity. We demonstrated that total AF protein was lower for LGA infants compared with AGA infants. We also established an important relation between concentrations of AF protein, measured early in the 2nd trimester, and subsequent infant birth weight. Multiple regression using birth-weight-for-gestational-age (39) showed that AF total protein concentration was a negative, not a positive, independent predictor of both birth weight and birth-weight-for-gestational-age. Finally, we provided evidence that total AF protein concentrations differed by colorimetric assay.

Our contrasting results from each of the 3 assays were similar to other reports in the scientific literature: Kirazov (48) in membrane-containing fractions, Keller and Neville (49) in human milk, and Jenzano et al. (50) in human saliva. Similar to our results, all of these previous studies found that the Lowry and BCA assays yielded almost identical mean concentrations, whereas the Bradford assay gave the lowest concentrations. It was suggested that these differences occur because of differences in interfering substances with each assay (38,51,52). In general, the Bradford assay is highly dependent upon the presence of arginine and lysine residues (38), whereas the BCA and Lowry assays are dependent upon the amino acids tryptophan, tyrosine, cysteine, and cystine, and the presence of the peptide bond (38). However, arginine and lysine reportedly are the most abundant amino acids in AF, whereas tryptophan and tyrosine are present in much smaller quantities (4); this would have predicted higher AF concentrations with the Bradford assay, which did not occur. We suggest that the basic alkaline properties of our AF matrix (i.e., mean pH = 7.97 ± 0.01) more likely interfered with the Bradford assay. However, why the Lowry assay was associated with birth weight and the BCA assay was not requires further investigation given the similarities in assay procedures.

All 3 biochemical methods detected differences in AF protein concentrations among the birth-weight-for-gestational-age categories (<10%, 10–90%, and >90%) with LGA infants having lower AF protein concentrations in the 2nd trimester; no significant difference was found when the infants were classified by weights that were not corrected for gender and gestational age. Our data showed in a large population of healthy pregnant women that AF total protein, measured by the Lowry method, was negatively associated with infant birth weight. This could be a result of specific protein components in AF, some of which are negatively correlated with fetal growth (25,26,53–55). Studies have reported that high concentrations of IGF-BP1 are associated with SGA infants, whereas low IGF-BP1 concentrations are associated with higher birth weight infants (54,55). It was proposed that high concentrations of IGF-BP1 could limit the availability of IGF-1 to the placenta (24). Negative relations with birth weight were also found with EPO because the abundance of this protein is indicative of fetal hypoxia (25,26). High AF interleukin-10 concentrations were similarly associated with SGA infants (53) and could be associated with higher rates of infection and hence lower growth rates given the higher metabolic requirements in utero. Another possible explanation for a negative relation between total AF protein and birth weight is that AF total protein may be modified by AF volume in such a way that higher AF protein concentrations occur because of limited AF volume expansion; it may indicate poor placental perfusion, which is associated with low-birth-weight infants (56). However, in our favor, there were very few infants < 2500 g, usually associated with low amniotic fluid volumes and low AFIs (amniotic fluid indices). The majority of our infants were AGA or LGA infants, both of which are relatively unaffected by changes in AFI and oligohydramnios (56) at least in the 3rd trimester when it is most often measured. However, this may or may not be physiologically similar to the earlier stages of development in our study. Another possibility is that AF proteins are found in lower concentrations in AGA and LGA infants because of increased amniotic fluid swallowing and increased absorption in these larger infants (16). Despite our inability at this time to differentiate among these possibilities, we will continue to try to determine which, if any, of the individual proteins such as hormones and growth factors have important positive relations with fetal growth and could be used as indicators of nutritional status. In addition, we must establish which AF proteins will continue to show a negative relation with fetal growth and therefore could be used as important biomarkers of fetal development and metabolic maturity. Thus, despite the large number of proteins in AF, our results demonstrate that as a family, AF proteins measured early in the 2nd trimester can be linked to infant birth weight and may provide interesting possibilities as early prognosticators of fetal growth and development in utero.


   FOOTNOTES
 
1 Supported by the National Sciences and Engineering Research Council (NSERC) of Canada. Back

3 Abbreviations used: AF, amniotic fluid; AFI, amniotic fluid index; AGA, appropriate-for-gestational age; BCA, bicinchoninic acid solution; EPO, erythropoietin; IGF-BP1, insulin-like growth factor binding protein 1; LGA, large-for-gestational-age; SGA, small-for-gestational-age. Back

Manuscript received 26 January 2004. Initial review completed 16 February 2004. Revision accepted 29 April 2004.


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 DISCUSSION
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D. K. Tisi, X.-J. Liu, L. J. Wykes, C. D. Skinner, and K. G. Koski
Insulin-Like Growth Factor II and Binding Proteins 1 and 3 from Second Trimester Human Amniotic Fluid Are Associated with Infant Birth Weight
J. Nutr., July 1, 2005; 135(7): 1667 - 1672.
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