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The Journal of Clinical Endocrinology & Metabolism Vol. 85, No. 1 85-88
Copyright © 2000 by The Endocrine Society

Original Studies

Plasma Apolipoprotein A-I and B Concentrations in Growth-Retarded Fetuses: A Link between Low Birth Weight and Adult Atherosclerosis

Nebojsa Radunovic, Edward Kuczynski, Todd Rosen, Jelena Dukanac, Spasoje Petkovic and Charles J. Lockwood

Obstetrical and Gynecological Clinic of the University of Belgrade School of Medicine (N.R., J.D., S.P.), 1000 Belgrade, Yugoslavia; and the Department of Obstetrics and Gynecology, New York University School of Medicine (E.K., T.R., C.J.L.), New York, New York 10016

Address all correspondence and requests for reprints to: Dr. Charles J. Lockwood, Department of Obstetrics and Gynecology, New York University School of Medicine, 550 First Avenue, New York, New York 10016. E-mail: charles.lockwood{at}med.nyu.edu


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Apolipoprotein B is elevated in growth-retarded compared with normally grown fetuses, demonstrating a link between low birth weight and risk of subsequent atherosclerosis. Increased apolipoprotein B levels and an elevated apolipoprotein B to A-I ratio are predictors of atherogenesis. Elevated apolipoprotein B levels in young adults have been linked to atherosclerosis in later life, whereas impaired fetal growth has been linked to higher than normal apolipoprotein B levels in adulthood. We conducted this research to test the hypothesis that circulating apolipoprotein A-I and B concentrations differ in growth-retarded compared with normal fetuses. Fetal umbilical plasma samples were obtained at diagnostic cordocenteses in 18 growth-retarded and 23 normally grown fetuses. Levels of apolipoprotein A-I and B were measured by turbidimetric assay. There were no differences in median (range) plasma apolipoprotein A-I concentrations between growth-retarded and normal fetuses [0.61 (0.30–1.42) vs. 0.60 (0.30–1.63) g/L, respectively; P = 0.94]. In contrast, we found significantly higher plasma apolipoprotein B levels in growth-retarded vs. normal fetuses [0.62 (0.37–1.84) vs. 0.40 (0.16–1.47) g/L, respectively; P < 0.001]. Moreover, the ratio of apolipoprotein B to A-I was significantly higher in growth-retarded than in normal fetuses [1.00 (0.38–2.42) vs. 0.53 (0.31–1.80); P = 0.005]. Levels of apolipoprotein B are elevated in growth-retarded fetuses, suggesting a linkage between low birth weight and adult-onset atherosclerosis.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
THE APOLIPOPROTEINS are important determinants of the metabolism and structure of plasma lipoproteins. Apolipoprotein A-I is a component of high density lipoproteins and an activator of plasma lecithin/cholesterol acyltransferase. Apolipoprotein B contains ligands for the receptor-mediated endocytosis of lipoproteins and is an essential component of chylomicrons and low density lipoproteins (LDL) (1). Increased apolipoprotein B levels and an elevated apolipoprotein B to A-I ratio are considered to be the most sensitive predictors of atherogenesis (2). Indeed, elevations in LDL, cholesterol, and apolipoprotein B levels in young adults have recently been linked with cardiovascular disease in later life (3).

Impaired fetal growth has been associated with elevated serum cholesterol and apolipoprotein B concentrations in adult life (4). Levels of apolipoprotein A-1 and B have been measured in fetuses displaying normal growth (5), but there are no data available on circulating fetal levels of apolipoproteins in growth-retarded fetuses. Therefore, we designed this study in an effort to determine how early altered apolipoprotein profiles could be related to abnormal growth. To accomplish this, we measured plasma concentrations of apolipoprotein A-I and B in growth-retarded and normally grown fetuses.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Participants were recruited from an ethnically homogeneous population of women attending the obstetrical clinic at the University of Belgrade School of Medicine who were scheduled to undergo diagnostic cordocentesis. Demographic and obstetrical characteristics were collected at the time of the procedure. A power analysis indicated the need for 18 participants in each fetal growth group, as described below. We therefore obtained serum samples from 18 growth-retarded fetuses as well as 23 consecutive fetuses displaying appropriate growth at similar gestational ages. The growth-retarded fetuses were identified on the basis of an ultrasonographic estimate of fetal weight less than the 10th percentile for a given gestational age that was subsequently confirmed at delivery (6). Gestational age was based on menstrual dates confirmed by an ultrasound examination performed between 18–20 weeks. Fetal blood samples were obtained at diagnostic cordocentesis to assess karyotype, analyze fetal arterial blood gas, or rule out fetal infection. None of these fetuses was aneuploid, acidotic, or infected. Maternal blood samples were obtained from the antecubital vein before the procedure. Exclusion criteria were maternal diabetes, hypertension, cigarette smoking, and taking medications other than prenatal vitamins or iron, illicit drugs, or steroids. Informed consent was obtained from all patients enrolled in the project, and the hospital ethics committee approved the study.

Cordocenteses were performed under strict aseptic conditions using a 20-gauge 15-cm spinal needle, which was guided into the umbilical vessel at the placental insertion by means of a 3.75-MHz convex ultrasound probe (Toshiba SSA 90; Toshiba Medical Systems S.R.L., Rome, Italy). Local anesthesia (1% lidocaine) was employed without maternal sedation. After satisfactory umbilical access was achieved, 3 ml fetal blood were obtained for diagnostic purposes. Immediately after obtaining the blood sample, 0.5 ml normal saline was injected to ascertain whether the sample was obtained from the umbilical artery or vein. The absence of maternal blood or amniotic fluid contamination was confirmed by Kleihauer-Betke analysis and assay for coagulation factor V, respectively. Blood was collected in heparinized tubes, and plasma was extracted by centrifugation at 1000 x g for 10 min at 4 C and stored at -20 C until assayed for levels of apolipoprotein A-I and B.

Apolipoprotein A-I and B concentrations were measured using a commercial turbidimetric assay (Roche Molecular Biochemicals, Indianapolis, IN). Intra- and interassay coefficients of variation were less than 5.0%. The sensitivity of this assay was 0.2 g/L for apolipoprotein A-I and 0.2 g/L for apolipoprotein B. The assay had less than 1% cross-reactivity with other apolipoproteins. To determine total triglyceride, cholesterol, high density lipoprotein, and LDL levels, we employed standard colorimetric assays (Randox Laboratories Ltd., Antrim, UK).

We performed a prospective power analysis to determine minimum sample size per group. As we were primarily interested in differences in apolipoprotein B levels in fetuses, we used our previously published data on apolipoprotein B levels in normal fetuses (5) to estimate the sample population mean. We established a minimal effect size of 33% as clinically meaningful. With {alpha} = 0.05 and ß = 0.20, 18 samples/group provides sufficient statistical power. All statistical analyses were performed using the JMP statistical software package (version 3.22, SAS Institute, Inc., Cary, NC), and included the Shapiro-Wilk test, Welch ANOVA, Wilcoxon rank sum test, and regression analysis. P < 0.05 was considered significant. Quantile box plots were used to illustrate the interquartile range (box), median value (horizontal line), and absolute range (range lines). Extreme points beyond 1.5 times the box length (interquartile range) appear as individual points.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
There were no procedure-related complications, including bradycardia, fetal death, preterm delivery, or infection, and all fetuses delivered uneventfully after 36 weeks. Table 1Go summarizes demographic and obstetrical characteristics as well as apolipoprotein levels among mothers with normally grown compared with those in mothers with growth-retarded fetuses. As expected, there were significant differences in fetal birth weight between the study and control groups. Maternal parity and age also differed between groups, consistent with published observations that primiparous and younger mothers tend to have smaller infants (7, 8). No statistically significant differences were noted in concentrations of either apolipoprotein A-I or B among mothers with growth-retarded compared with normally grown fetuses.


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  		Table 1. Demographic and obstetrical characteristics of normal compared with growth-retarded fetuses

 
There was no difference in median (range) plasma apolipoprotein A-I concentrations between growth-retarded and normal fetuses [0.61 (0.30–1.42) vs. 0.60 (0.30–1.63) g/L, respectively; P = 0.94]. In contrast, plasma apolipoprotein B concentrations in growth-retarded fetuses were significantly higher than those in normal fetuses [0.62 (0.37–1.84) vs. 0.40 (0.16–1.47) g/L, respectively; P < 0.001; Fig. 1Go]. The ratio of apolipoprotein B to A-I was significantly higher in growth-retarded compared with normal fetuses [1.00 (0.38–2.42) vs. 0.53 (0.31–1.80); P = 0.005; Fig. 2Go]. There was no correlation between maternal and fetal apolipoprotein A-I or B levels (r = 0.05; P = 0.85 and r = -0.41; P = 0.12, respectively) among pregnancies with growth-retarded fetuses.



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  		Figure 1. Quantile box plots of plasma apolipoprotein (Apo) A-I (left) and B (right) levels in fetuses with intrauterine growth retardation (IUGR) compared with those in fetuses with normal growth. Differences were assessed by Wilcoxon rank sum test. Apo B differences are significant at P < 0.001.

 


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  		Figure 2. Quantile box plots of plasma apolipoprotein (Apo) B to A-I ratio in fetuses with intrauterine growth retardation (IUGR) compared with that in fetuses with normal growth. Differences were assessed by Wilcoxon rank sum test. P = 0.005.

 
Among normal and intrauterine growth-retarded fetuses, no significant correlation was found between fetal apolipoprotein A-I or B and gestational age. Among normal and growth-retarded fetuses there were no differences in either apolipoprotein A-I or B levels between samples obtained from the umbilical artery compared with those from the umbilical vein (Table 2Go). This finding indicates that the placenta does not significantly alter plasma apolipoprotein A-I or B levels.


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  		Table 2. Apo A-I and Apo B concentrations in the umbilical arteries and veins of normal growth and growth-retarded fetuses

 
Total fetal triglyceride levels were positively correlated with gestational age, but did not differ between the growth-retarded and normal growth groups (Fig. 3Go). Total triglyceride values for each group are presented in Table 3Go.



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  		Figure 3. Scattergram of total triglycerides by gestational age in normal (+) and IUGR (open boxes) fetuses. Triglyceride concentrations were positively correlated with gestational age in both normal (solid line) and IUGR (dashed line) fetuses by linear regression analysis, but the two groups did not differ significantly from each other.

 

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  		Table 3. Total triglyceride concentrations in normal growth and growth-retarded fetuses (grams per L)

 

   Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We have previously reported that concentrations of fetal plasma apolipoprotein A-1 and B do not correlate with gestational age and are substantially lower than matched maternal levels in uncomplicated pregnancies (5). We now report a significant difference in apolipoprotein B concentrations and the ratio of apolipoprotein B to A-I in growth-retarded compared with normally grown fetuses.

Recently, Barker et al. reported an inverse correlation of birth weight and neonatal abdominal circumference with adult cholesterol, LDL, and apolipoprotein B levels (4). Our findings suggest that the association between aberrant lipoprotein metabolism and low birth weight is present by the time intrauterine growth restriction is clinically evident. Others have demonstrated that abnormal lipoprotein profiles in childhood persist into adult life (9, 10, 11). Additionally, both the prevalence and severity of carotid artery atherosclerosis in later life have been linked to lower birth weights (12), and a comprehensive Swedish cohort study found a strong relationship between impaired fetal growth and subsequent cardiovascular disease mortality (13). Taken together, these findings strongly support the Barker hypothesis that fetal growth restriction is associated with a chronic pattern of atherogenic lipoprotein metabolism. The absence of any significant difference in total triglyceride levels between the two groups in our study further supports a constitutional basis for the differences in apolipoprotein metabolism that we observed.

The literature on neonatal lipoprotein concentrations and growth is somewhat inconsistent. Andersen et al. observed elevated levels of serum LDL in growth-retarded neonates (14). Moreover, Low and colleagues found ethnic differences in neonatal umbilical vein apolipoprotein B levels, which positively correlated with adult coronary artery disease risk (15). In contrast, Spencer and associates noted no differences in neonatal umbilical vein apolipoprotein B levels or the ratio of apolipoprotein B/A-I in growth-retarded compared with normally grown neonates (16). Such differences in neonatal results may reflect ethnic heterogeneity (15), failure to correct for cigarette smoking (17), and/or the stress of labor and delivery (18). These factors underscore the added value of our present study, as we collected fetal samples from an ethnically homogeneous, nonsmoking population.

The mechanism for the occurrence of fetal growth retardation-associated apolipoprotein B elevations and the persistence of this atherogenic milieu into childhood and throughout life is currently unknown. Perhaps the stress resulting from fetal growth retardation establishes a life-long irreversible atherogenic lipoprotein profile driven by chronic activation of the hypothalamic-pituitary-adrenal axis. In support of this position, fetal growth retardation has been associated with increased fetal cortisol levels (19). Secondly, glucocorticoid therapy has been shown to result in increased neonatal cord blood apolipoprotein B concentrations (20), and glucocorticoids have been shown to enhance apolipoprotein B messenger ribonucleic acid synthesis in cultured hepatocytes (21). Hormone-bound glucocorticoid receptor can cause stable changes in chromatin architecture (22), which is a time-dependent process that is fundamental in modulating gene activity (23). Thus, if the fetus is exposed to prolonged periods of stress in utero due to uteroplacental insufficiency and growth retardation, chromatin remodeling represents a potential mechanism by which elevated cortisol levels could permanently alter gene expression. This mechanism could account for the dual observations that men with low birth weights have increased fasting plasma cortisol levels as adults (24) as well as an atherogenic lipoprotein profile (4).

Alternatively, a common molecular defect could independently lead to both fetal growth retardation and an atherogenic lipoprotein profile. The LDL receptor mediates the uptake of apolipoprotein B into cells, whereas mutations in the LDL receptor and related proteins (LRP) lead to premature atherosclerosis (25). Trophoblasts express high levels of LDL receptor and related proteins (26). However, LRP also serves as a ligand for the complex of urokinase-type plasminogen activator (uPA), its inhibitor, and the uPA cell surface receptor (27). In this capacity, LRP facilitates recycling of the uPA receptor to restore active uPA on the cell surface. The internalization of receptor-bound inactivated uPA is a crucial characteristic of invasive cells, including trophoblasts (28, 29, 30, 31). Thus, a defect in the LDL receptor family of proteins could lead to both impaired trophoblast invasion, the characteristic placental lesion associated with fetal growth retardation, as well as elevated fetal, neonatal, childhood, and adult apolipoprotein concentrations. Indeed, trophoblast cells derived from preeclamptic patients, a disorder also associated with shallow trophoblast invasion and fetal growth retardation, display reduced cell surface uPA activity (32).

In summary, we have shown that growth-retarded fetuses display an atherogenic milieu that appears to persist into adulthood and contributes to the strong association between fetal growth retardation and adult atherosclerosis. Further research is needed to determine the exact mechanism(s) for this association.

Received January 6, 1999.

Revised September 22, 1999.

Accepted October 3, 1999.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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