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Longitudinal Study of Serum Placental GH in 455 Normal Pregnancies: Correlation to Gestational Age, Fetal Gender, and Weight

Department of Growth and Reproduction (M.C., A.J., A.-M.A., K.M.M., J.H.P., N.E.S.), Righospitalet, University Hospital of Copenhagen, DK-2100 Copenhagen, Denmark; Department of Gynecology and Obstetrics (L.S., S.O.S.), University Hospital of Copenhagen, Righospitalet and Fredriksberg Hospital, DK-2100 Copenhagen, Denmark; and Department of Biostatistics (J.H.P.), The Panum Institute, University of Copenhagen, DK-2200 Copenhagen, Denmark

Address all correspondence and requests for reprints to: Marla Chellakooty, M.D., Department of Growth and Reproduction, Section 5064, Rigshospitalet Blegdamsvej 9, 2100 Copenhagen, Denmark. E-mail: . RH04632{at}rh.dk

Abstract

Placental GH is thought to be responsible for the rise in maternal IGF-I during pregnancy and is considered to be important for fetal growth. In this prospective longitudinal study of healthy pregnant women, we investigated determinants of placental GH in maternal serum. Serum was obtained from 455 women with normal singleton pregnancies at approximately 19 and 28 wk gestation. Serum placental GH concentrations were measured by a highly specific immunoradiometric assay, and fetal size was measured by ultrasound. Data on birth weight, gender, prepregnancy body mass index (BMI), parity, and smoking habits were obtained from medical records. Serum placental GH concentrations were detectable in serum from all women as early as 14 wk gestation and increased during pregnancy in all individuals (P < 0.001). Placental GH levels at second examination were found to be higher in women carrying female fetuses [median, 9.0 ng/ml; 95% confidence interval (CI), 4.7–23.0] compared with women carrying male fetuses (median, 8.2 ng/ml; 95% CI, 3.96–19.4; P = 0.004). Similarly, the increase in placental GH between 19 and 28 wk gestation was significantly larger in female fetus bearers than in male fetus bearers (P = 0.002). Placental GH at second examination was positively correlated with gestational age (P = 0.002) and negatively correlated with prepregnancy BMI (P = 0.039). Placental GH correlated with fetal weight at approximately 28 wk gestation (P = 0.002) but did not predict birth weight at term. Our study supports the role of maternal placental GH in the regulation of fetal growth. In conclusion, we found that 1) placental GH levels correlated significantly with fetal size at 28 wk gestation; 2) GH levels were measurable in serum from all women as early as 14 wk gestation; 3) maternal prepregnancy BMI and smoking were determinants of placental GH levels, although their specific effects on the serum maternal levels of placental GH remain to be seen; and 4) women carrying female fetuses have significantly higher placental GH levels compared with women carrying male fetuses at 28 wk gestation.

THE ENDOCRINE MECHANISMS involved in the regulation of intrauterine growth and early postnatal growth are poorly understood. Recently, a new GH variant produced in the placenta, named placental GH, has been recognized (1). The hormone may participate in the regulation of intrauterine growth, although its precise function is still to be elucidated.

Placental GH is produced by the syncytiotrophoblasts (2, 3) as the major protein product of the GHV gene (1). Placental GH is secreted into the maternal circulation and cannot be detected in fetal circulation or cord serum from the newborn. Placental GH binds to the circulating GH binding protein (4) and to GH receptors found in placental tissues and rabbit liver (5). Its continuous secretion from the placenta progressively increases throughout gestation from approximately 20 wk gestation, and it is thought to suppress the pulsatile secretion of pituitary GH (either directly or via IGF-I) although this has not yet been demonstrated (6). This nonpulsatile manner in which placental GH is secreted makes it possible to investigate the hormone level in one sample. The increase in placental GH throughout gestation is found to be associated with a progressive rise of IGF-I levels in maternal serum and is thought to be a potential regulator of IGF-I in human pregnancies (7, 8). In pregnancies with intrauterine growth retardation (IUGR), placental GH and maternal IGF-I levels are found to be significantly lower compared with levels found in normal pregnancies (8, 9). Because placental GH does not cross the placenta into the fetal circulation, its effect on fetal growth is considered to be indirectly mediated by the effect on maternal IGF-I and thereby regulation of the substrate supply to the fetus (10).

Early studies evaluated the pregnancy-associated rise in placental GH by an indirect method based on its reactivity with two monoclonal antibodies (MAb:K24 and Mab5B4) raised against purified pituitary GH (11). The Mab5B4 antibody reacts with the N-terminal epitope of both pituitary and placental GH, and the MAb:K24 antibody reacts with an internal epitope that only recognizes pituitary GH. The difference in the results obtained by the two assays gives an estimate of serum placental GH concentrations. With the advent of a specific assay (12) that recognizes a distinct epitope for placental GH, this present study was carried out to establish reference ranges for circulating placental GH in 455 normal pregnant women and to investigate determinants of placental GH serum levels in pregnancy.

Materials and Methods

Study participants and design

All pregnant women coming for a routine ultrasound examination in an outpatient clinic during the period November 1, 1996, to June 1, 1998, were asked to participate if gestational age determined by the biparietal diameter was between 14 and 22 wk gestation. Nine hundred seventy pregnant women were consecutively recruited. A nonfasting blood sample was taken from an antecubital vein, and participants were scheduled to come for a second ultrasound examination at approximately 28 wk gestation when a second blood sample was drawn. The same team of trained ultrasound nurses examined all participants using an Aloka 2000 ultrasonographic apparatus (3.5 and 5 MHz convex transducer; Aloka, Tokyo, Japan). Data on a subcohort of 455 healthy singleton pregnancies were selected according to the following criteria: systolic blood pressure below 120 mm Hg and diastolic blood pressure below 90 mm Hg, no other pregnancy complications, and a maternal prepregnancy body mass index (BMI) below 25.5. All pregnancies resulted in singletons born between 37 and 42 wk gestation with birth weights greater than -22% (-2 SD) of expected birth weight corrected for gestational age (13). Maternal height, prepregnancy weight, age, parity, and smoking habits were obtained from medical records. The study was approved by the local ethics committee (ref. no. KF 02-125/95) and the Danish Registry Agency, and all participants gave their written informed consent.

Laboratory methods

Serum samples were separated by centrifugation and then stored at -20 C until analysis. Placental GH levels were assayed using two specific monoclonal antibodies in a solid phase ¹²⁵I-labeled immunoradiometric assay (Biocode, Liege, Belgium). In our laboratory, the intra-assay coefficient of variation was 7.9% (at 24.6 ng/ml; n = 20) and 6.3% (at 5.0 ng/ml; n = 20); the interassay coefficient of variation was 6.1% (at 4.1 ng/ml; n = 20), 9.7% (at 22.2 ng/ml; n = 20), and 8.1% (at 35.6 ng/ml; n = 20). The limit of detection was less than 0.1 ng/ml defined as zero standard +3 SD.

Statistics

Placental GH levels were subjected to a logarithmic transformation to correct for the marked right skewness and to obtain approximate normality. The independent t test was used to compare groups. The first measurement, the second measurement, and the change from first to second measurement in placental GH levels were studied in linear regression models. Covariates included sex of the fetus, gestational age at the time of blood sampling and at birth, mother’s age, prepregnancy BMI, parity, and smoking habits. Fetal weight and birth weight were also studied using linear regression models with the above mentioned covariates. Parameter estimates are given in percentages with negative or positive values indicating either a negative or positive correlation, respectively. BMI was calculated by using the following formula: BMI (kg/m²) = weight (kg)/height² (m²). The final models were validated using standard test of the residuals.

Reference curves for the highly skewed distribution of the placental GH levels as a function of gestational age were estimated. The curves represent the 2.5 percentile, the median, and the 97.5 percentile. The curves were obtained by a locally weighted regression quantile (14) that takes into account the marked right skewness of the data.

Results

Details of the study population are shown in Table 1.

Placental GH levels were detectable in all pregnant women as early as 14 wk gestation. Furthermore, placental GH increased significantly from first measurement (19 wk gestation) to second measurement (28 wk gestation) in all women (P < 0.001). The serum placental GH levels for both female fetus bearers and male fetus bearers are shown in relation to gestational age in Fig. 1.

View larger version (13K): [in this window] [in a new window]   Figure 1. Maternal serum levels of placental GH in pregnant women bearing male (left) and female (right) fetuses, respectively, in relation to gestational age at time of blood sampling. Solid lines represent the 2.5, 50, and 97.5 percentiles.

Placental GH increased to 14% higher levels at 28 wk gestation in women bearing female fetuses compared with women bearing male fetuses (mean difference, 0.8 ng/ml; 95% CI, 0.33–1.95; P = 0.006) (Fig. 1 and Table 1). Taking gestational age, parity, mother’s age, smoking, prepregnancy BMI, and fetal weight into account, the levels of placental GH in women bearing female fetuses remained significantly higher by 4.9% (95% CI, 1.6–7.8%; P = 0.004). By contrast, fetal size as determined by ultrasound (39 g; 95% CI, 18.04–79.49; P = 0.002) as well as birth weight (160 g; 95% CI, 62.75–230.37; P = 0.001) was significantly higher in male fetuses compared with female fetuses (Table 1).

Determinants of placental GH

At first examination, gestational age was positively (P = 0.002) associated and maternal prepregnancy BMI was negatively (P = 0.025) associated with placental GH levels in a multivariate analysis (Fig. 2). Mother’s age, parity, smoking, birth weight, and gender of the fetus were not correlated to placental GH at first examination (Table 2).

View larger version (19K): [in this window] [in a new window]   Figure 2. Individual longitudinal increase in serum placental GH levels in mothers bearing male fetuses (left) and female fetuses (right) as a function of gestational age.

The determinants of the increase in placental GH ( placental GH) levels are also shown in Table 2.

Placental GH levels and fetal size

Fetal size determined by ultrasound was significantly associated with placental GH levels (P = 0.002) at second examination in a multivariate analysis with a parameter estimate of 5.07 and 95% CI of 1.86–8.29. When factors such as mother’s age, parity, smoking, gender of the fetus, and prepregnancy BMI were corrected for, placental GH remained significantly positively correlated with fetal size. However, no association was found (P = 0.384) between mid-gestation placental GH levels and birth weight (Table 3).

In the present longitudinal study of 455 pregnant women with normal pregnancies, we have demonstrated that placental GH levels were detectable in serum of all pregnant women at approximately 14 wk gestation and increased significantly in all women at 28 wk gestation. At 28 wk gestation, maternal placental GH levels were significantly associated with fetal weight determined by ultrasonography and influenced by maternal prepregnancy BMI and smoking. In addition, we found a significant influence of fetal gender; women bearing female fetuses had higher placental GH levels compared with women bearing male fetuses.

Placental GH is likely to have an effect on placental substrate distribution and metabolism through its regulation of the maternal IGF axis, although this remains to be demonstrated. In this study, we found maternal placental GH serum levels at 28 wk gestation to be positively correlated with fetal weight as determined by ultrasound, which to our knowledge has not previously been shown. Previous studies (15, 16, 17) have primarily related third trimester placental GH levels with birth weight and not with estimated fetal weight earlier in pregnancy (second trimester) as done in our present study. Nevertheless, decreased third trimester placenta GH levels [determined by indirect (15) or direct assays (16, 17)] were found in IUGR pregnancies in those studies. Placental GH did not predict normal birth weight at term in our study, but this could be due to the fact that we only included infants with normal birth weights.

Interestingly, we found a significant impact of fetal gender on maternal levels of placental GH in mid-gestation, after controling for an apparent difference in gestational age at first examination between male and female fetus bearers. This was recently shown in 87 pregnant women in whom blood samples were drawn at the onset of labor (17). However, placental GH levels decrease with the onset of labor (9), which may influence those results. Several studies have observed that female fetus bearers have higher human CG levels throughout late gestation and lower alfa-fetoprotein serum levels compared with male fetus bearers (18, 19, 20). Studies of human placental lactogen have found higher levels in pregnancies with female fetuses both in cord blood and in the maternal circulation, although the gender-related differences are not significant in the maternal circulation (21, 22). In contrast, estriol and prolactin levels do not seem to differ during pregnancy according to gender of the fetus (21, 23).

Because placental GH is produced by the syncytiotrophoblast, one could speculate whether the gender difference in maternal serum levels of placental GH is due to a difference in placental size in women bearing female fetuses and male fetuses, respectively. Unfortunately, data on placental size was not obtained in this study, because medical records of placental weight were inconsistent. However, other studies have shown that placental weight is positively associated with birth weight and tends to be higher in male than in female infants (24, 25). Consistent with other studies, we found a significant gender difference in birth weights, with male infants being heavier at birth than female infants.

Smoking alters the mechanical properties of the stem villous arteries in the placenta (26), which compromises fetal placental blood flow and results in IUGR (27). However, we found significantly increased placental GH levels in the 65 women who smoked during pregnancy, which is in contrast to the findings of Coutant et al. (17). We believe the data must be evaluated cautiously due to the limited numbers of smokers.

We found a negative association between prepregnancy BMI and placental GH. It is interesting to note that although the mechanisms may be different, similar correlations have been recorded for BMI and the 24-h integrated pituitary GH secretion, obese individuals having low GH secretion that is restored upon massive weight loss (28).

Limited data exist on the regulation of placental GH, and so far only serum glucose has been found to be involved in the regulation of placental GH secretion. In vitro experiments have demonstrated that secretion of placental GH from human placenta explants and trophoblast cultures was strongly inhibited by glucose concentrations (29). These data have been supported by a few in vivo studies of acute changes in glucose levels in pregnant women. Thus, placental GH was inhibited during an oral glucose tolerance test in women with gestational diabetes (30) and stimulated in pregnant women with insulin-dependent diabetes mellitus during a hyperinsulinemic hypoglycemic clamp (31). Therefore, increased glucose levels due to the relative insulin resistance seen in pregnant women could in part explain our findings of low placental GH levels with increasing prepregnancy BMI.

This study provides normal ranges for maternal serum placental GH concentrations in second trimester pregnancies, based on 455 women with normal pregnancies using a specific assay for placental GH.

In conclusion, we found that 1) placental GH levels correlated significantly with fetal size at 28 wk gestation; 2) placental GH levels were measurable in serum from all women as early as 14 wk gestation; 3) maternal prepregnancy BMI and smoking were determinants of placental GH levels, although their specific effects on the maternal levels of serum placental GH remain to be seen; and 4) women carrying female fetuses have significantly higher placental GH levels compared with women carrying male fetuses at 28 wk gestation.

Acknowledgments

We thank Prof. Georges Hennen and Biocode (Liege, Belgium) for their support in providing the assay kits.

Footnotes

This study was funded by a European Union grant (contract QLK4-1999-01422) and by The Danish Medical Research Council (Grant 9700833).

Abbreviations: BMI, Body mass index; CI, confidence interval; IUGR, intrauterine growth retardation.

Received October 15, 2001.

Accepted February 21, 2002.

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This Article Abstract Full Text (PDF) Submit a related Letter to the Editor Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Copyright Permission Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Chellakooty, M. Articles by Juul, A. Search for Related Content PubMed PubMed Citation Articles by Chellakooty, M. Articles by Juul, A.