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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2006-1281
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The Journal of Clinical Endocrinology & Metabolism Vol. 92, No. 2 681-684
Copyright © 2007 by The Endocrine Society

Glucose and Lipid Metabolism in Small-for-Gestational-Age Infants at 72 Hours of Age

Xinli Wang, Yunpu Cui, Xiaomei Tong, Hongmao Ye and Song Li

Department of Pediatrics, Peking University Third Hospital, Beijing 100083, People’s Republic of China

Address all correspondence and requests for reprints to: Xinli Wang, Ph.D., Department of Pediatrics, Peking University Third Hospital, Beijing 100083, People’s Republic of China. E-mail: Xinli_Wang1217{at}yahoo.com.cn.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Context: Reduced birth weight is associated with increased risk for the insulin resistance syndrome. Part of this risk is hypothesized to originate from intrauterine growth retardation.

Objective: The aim of this study is to determine whether or not the components of the insulin resistance syndrome are associated with reduced fetal growth.

Design: This was a case-control study.

Setting: The study was conducted in Beijing, China.

Participants: Included in this study were 296 singleton neonates (177 males and 119 females), including 76 (37 preterm and 39 full-term newborns) classified as small for gestational age (SGA) and 220 who were appropriate for gestational age (AGA) (84 preterm and 136 full-term newborns).

Main Outcome Measures: The main outcome measures were postabsorptive glucose, insulin, and lipids levels on the third day after birth.

Results: Both full-term and preterm SGA neonates had higher insulin concentrations (mean ± SEM, 17.11 ± 1.15 vs.6.80 ± 0.62 µIU/ml in full-term, P < 0.01; 11.99 ± 1.18 vs.8.37 ± 0.78 µIU/ml in preterm, P = 0.03), insulin to glucose ratios (4.48 ± 0.37 vs. 1.78 ± 0.20 in full-term, P < 0.01; 3.28 ± 0.38 vs. 2.30 ± 0.26 in preterm, P = 0.03), triglycerides (2.29 ± 0.23 vs.1.57 ± 0.13 mmol/liter in full-term, P < 0.01; 2.27 ± 0.16 vs. 1.34 ± 0.11 mmol/liter in preterm, P < 0.01), total cholesterol (2.35 ± 0.12 vs. 1.82 ± 0.22 mmol/liter in full-term, P = 0.04; 2.57 ± 0.22 vs. 1.95 ± 0.15 mmol/liter in preterm, P = 0.02), and low-density lipoprotein cholesterol (2.11 ± 0.58 vs. 1.24 ± 0.61 mmol/liter in full-term, P = 0.01; 1.87 ± 0.60 vs. 1.38 ± 0.59 mmol/liter in preterm, P < 0.01) concentrations than did AGA neonates; however, they had similar glucose levels. Among AGA infants, insulin concentration, insulin to glucose ratios, and lipids levels did not significantly differ between full-term and preterm babies.

Conclusions: In this study, SGA neonates displayed profiles suggestive of lower insulin sensitivity and less favorable lipid metabolism in the early postnatal period.


   Introduction
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 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
A NUMBER OF epidemiological studies in different races and ethnic groups have shown a consistent association between low birth weight and hypertension, coronary heart disease, and type 2 diabetes mellitus in adult life (1, 2, 3). Altered sensitivity to insulin has also been related to low birth weight (2). These findings have led to the "fetal origins hypothesis," which suggests that an adverse intrauterine environment during a critical period of development could program or imprint the development of fetal tissues and organs, and permanently determine responses that produce later dysfunction and disease (4, 5). The nature of this programming is not yet clear, but long-term, tissue-specific modifications of insulin sensitivity may play a role (6).

According to the fetal origins hypothesis, the result of metabolic and endocrine programming should be present during early postnatal life and infancy. More precisely, it can be expected that small-for-gestational-age (SGA) newborns should display lower insulin sensitivity compared with those who are appropriate for gestational age (AGA). Recently, impaired insulin sensitivity has been reported in children who were SGA (7, 8, 9, 10), but little is known about insulin sensitivity in newborn infants, especially the metabolism of lipids, which is an indicator of insulin action. The aim of this study was to investigate the metabolisms of glucose and lipids in SGA infants, including preterm infants, during the early neonatal period, and by means of measuring postabsorptive insulin, glucose, and the insulin to glucose ratio (insulin:glucose), to compare their insulin sensitivity to that of AGA infants.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
Study population

We defined an SGA infant as one having a birth weight below the 10th percentile of the local sex-specific distribution for gestational age, and an AGA infant as one having a birth weight between the 25th and 75th percentile of the local sex-specific distribution for gestational age. We selected singleton neonates who were delivered from April through December 2001, in the Department of Obstetrics of the Third Hospital, Peking University, and who had a 1-min Apgar score of more than 7 and a 5-min Apgar score of 10. The SGA neonates were selected from consecutive SGA deliveries, and the AGA neonates were randomly selected from newborns whose birth weights fulfilled the criteria outlined here. We excluded infants with congenital malformations, as well as those born to women with diabetes mellitus, gestational diabetes, chronic hypertension, or intrauterine infections. Parents were informed about the study and invited to participate; infants were included only after parents gave written informed consent. The study protocol was performed according to the Helsinki II Declaration and was approved by the Ethics Committee of Third Hospital, Peking University.

Anthropometric and laboratory analyses

Routine measurements of weight, length, head circumference, and chest circumference were performed at birth. Birth weight Z scores were computed using the following formula: Z = (x – mean)/SD, where x is the infant’s birth weight and mean and SD are the mean and SD for each gestational age and sex group in newborn babies from 15 cities in China.

Blood was obtained by heel-prick before feeding, and at least 2.5 h after the previous feed, between 0830 and 0930 h on the d 3 or 4 of life [each infant was given an infant formula milk meal (Nestle Nan1, Nestec Ltd., Vevey, Switzerland) after a 3- to 4-h fast since birth] and 15 µl whole blood were added to SureStep Test strips (LifeScan, Inc., Milpitas, CA) for glucose analysis, and 100 µl blood was collected into a heparinized container for insulin analysis. At same time, 2.0 ml of venous blood was drawn to measure serum lipid concentration in those neonates whose parents granted permission for investigators to obtain blood by venipuncture for lipid analysis. Anthropometric data from parents, as well as pregnancy and delivery events, were obtained from hospital clinic records.

Glucose concentration was measured by SureStep Plus System (LifeScan). Interassay and intraassay coefficients of variation for glucose were 0.9% and 1.8%, respectively. Insulin was measured by enzyme-amplified immunoassay using an active insulin ELISA Kit supplied by the Diagnostic Systems Laboratories, Inc. (Webster, TX). The detection limit of this assay was 0.26 µIU/ml in our laboratory, and the intraassay and interassay coefficients of variation were 2.6% and 5.2%, respectively. Total cholesterol, high-density lipoprotein cholesterol, and triglyceride concentrations were measured by using standard enzymatic methods in the Department of Laboratory Medicine, Third Hospital, Peking University. Low-density lipoprotein cholesterol (LDL-c) was calculated using the Friedewald-Fredrickson formula.

Statistical analysis

Data are expressed as means ± SEM or percent. Postabsorptive insulin data and insulin/glucose ratio[serum insulin (µIU/ml)/blood glucose (mmol/liter)] had skewed distributions and was log transformed for analysis. Differences in demographic characteristics and clinical measures between AGA and SGA neonates were investigated by means of unpaired Student’s t test for quantitative variables and the Fisher exact test for categorical variables. ANCOVA was used to compare the mean values of glucose, insulin, insulin:glucose ratio, and lipids between SGA and AGA neonates; sex and gestational age were included as covariates. All statistical analyses were performed using the SPSS for Windows 11.0 statistical software package (SPSS Inc., Chicago, IL). P ≤ 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
The study sample consisted of 296 singleton neonates (177 boys and 119 girls), including 76 SGA neonates (37 preterm and 39 full-term), and 220 AGA neonates (84 preterm and 136 full-term). The main characteristics of the AGA and SGA neonates and their parents according to gestational age are shown in Table 1Go. The SGA neonates were significantly smaller at birth than AGA neonates. Maternal and parental age and parental body mass index were not different between groups both in full-term and in preterm infants; however, maternal body mass index before pregnancy and weight gain during pregnancy were lower in SGA neonates compared with AGA neonates for both full-term and preterm neonates. Mothers of preterm babies were, on average, 14 months older than those of full-term infants (28.55 ± 4.90 yr, 27.39 ± 3.42 yr, respectively; P = 0.012).


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  		TABLE 1. Characteristics of AGA and SGA infants and their parents according to gestational age

 
Hypertension during pregnancy was significantly more common in preterm births (34.7%) than in full-term births (14.3%). In addition, a significantly larger proportion of mothers of SGA neonates were hypertensive during pregnancy than were mothers of AGA neonates, among both preterm and full-term deliveries.

Because the effects of a low birth weight on insulin and lipid variables were not significantly different in boys and girls, a pooled analysis, adjusted for sex, is presented. Figure 1Go shows mean plasma glucose, insulin, and insulin-to-glucose ratio for AGA and SGA neonates, according to gestational age. Plasma glucose levels were similar in the AGA and SGA groups, both for full-term and preterm infants; however, insulin levels and insulin-to-glucose ratios were significantly higher in the SGA groups than in the AGA groups, both for full-term (SGA value 17.11 ± 1.15 µIU/ml and AGA value 6.79 ± 0.62 µIU/ml, respectively; P < 0.01) and preterm infants (SGA value 11.99 ± 1.18 µIU/ml and AGA value 8.38 ± 0.78 µIU/ml, respectively; P < 0.05). In SGA neonates, insulin levels and the insulin-to-glucose ratio tended to be higher in full-term neonates than in preterm neonates (P = 0.01, 0.02, respectively). Among AGA neonates, the difference in insulin levels and the insulin-to-glucose ratio between full-term and preterm babies were not significant.


Figure 1
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  		FIG. 1. Insulin and glucose levels by AGA/SGA status and gestational age group (preterm/full term). Data represent means ± SEM. Sex and gestational age were controlled respectively in full-term and preterm neonates for in this analysis. To convert insulin to picomoles per liter, multiply by 6.94. Asterisks (*) indicate values that differ between AGA and SGA in term (**, P < 0.01). Triangles ({triangleup}) indicated values that differ between AGA and SGA in preterm ({triangleup}, P < 0.05).

 
Parents of 160 (54%t) neonates gave permission for venipuncture for lipid analysis. The mean birth weight of neonates whose parents consented to the lipid analysis and those whose parents did not was similar. Figure 2Go shows the mean lipid values for the AGA and SGA neonates according to gestational age. After adjusting for gestational age and sex, respectively, in full-term neonates and preterm neonates, SGA neonates had higher triglyceride, total cholesterol, and LDL-c levels than did AGA infants both among full-term and preterm neonates (triglyceride value 2.29 ± 0.23 vs. 1.57 ± 0.13 mmol/liter in full-term, P < 0.01; 2.27 ± 0.16 vs. 1.34 ± 0.11 mmol/liter in preterm, P < 0.01, total cholesterol value 2.35 ± 0.12 vs. 1.82 ± 0.22 mmol/liter in full-term, P = 0.04; 2.57 ± 0.22 vs. 1.95 ± 0.15 mmol/liter in preterm, P = 0.02, and LDL-c value 2.11 ± 0.58 vs. 1.24 ± 0.61 mmol/liter in full-term, P = 0.01; 1.87 ± 0.60 vs. 1.38 ± 0.59 mmol/liter in preterm, P < 0.01). Among AGA infants, lipids levels did not differ between full-term and preterm babies.


Figure 2
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  		FIG. 2. Mean lipid values by AGA/SGA status and gestational age group (full-term/preterm). Data represent means ± SEM. Sex and gestational age were controlled, respectively, in full-term and preterm neonates for in this analysis. Insulin data and insulin/glucose ratio were log-transformed for statistics to generate P values. Asterisks (*) indicate values that differ between AGA and SGA in term (*, P < 0.05; **, P < 0.01). Triangles ({triangleup}) indicate values that differ between AGA and SGA in preterm ({triangleup}, P < 0.05; {triangleup}{triangleup}, P < 0.01). TG, Triglyceride; TC, total cholesterol; HDL-c, high-density lipoprotein cholesterol.

 

   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
The best test of the fetal origins hypothesis would be to assess insulin sensitivity soon after birth, thereby ensuring that postnatal factors do not confound the analysis. The present investigation showed that a relationship between insulin sensitivity and birth weight does exist in the neonate. Both premature and term SGA neonates had higher insulin concentrations, insulin to glucose ratios, as well as triglyceride, total, and LDL-c concentrations, providing strong support for the fetal origins hypothesis.

Insulin sensitivity is usually defined as the ability of insulin to stimulate glucose uptake in its peripheral target tissues. Resistance to the actions of insulin results in overproduction of this hormone by the pancreatic ß-cells to maintain glucose homeostasis, with ensuing hyperinsulinemia (11). The "gold standard" for quantifying insulin sensitivity in vivo is the hyperinsulinemic euglycemic glucose clamp technique, in which insulin is measured under conditions of steady plasma glucose concentration, and in which glucose uptake can be measured as the glucose infusion rate during a constant infusion of insulin. This technique directly measures the effects of insulin on glucose utilization under steady-state conditions (12); however, it is not appropriate to perform in newborns. In this population, we are reliant on measures of fasting blood glucose and insulin, complemented by other indirect measures of insulin sensitivity, such as lipid concentrations, which have been found to reflect insulin action in a number of age groups, including newborn infants (13).

In the present study, glucose levels on d 4 were similar in the SGA and AGA neonates, whereas there were significantly higher insulin levels and insulin:glucose ratios in SGA neonates. This suggests that SGA infants require a higher insulin secretory response than AGA infants to maintain glucose homeostasis, consistent with reduced insulin sensitivity. The higher insulin levels in SGA infants suggest that insulin resistance may arise from fetal growth retardation rather than ß-cell dysfunction, which has been reported to be the first detectable event in the etiology of type 2 diabetes (14, 15). This ß-cell insufficiency is revealed only later in life in the presence of obesity, which further elevates the level of insulin resistance (16).

In addition to controlling plasma glucose concentration, insulin has other metabolic actions that were also modified in the SGA newborns. Serum triglyceride, total cholesterol, and LDL-c concentrations were higher in the SGA neonates than in AGA neonates, whereas high-density lipoprotein cholesterol concentrations were similar, suggesting a limited ability to clear intravenous lipids in SGA infants. These findings are in agreement with many previous studies in adults and children that show that low birth weight was significantly associated with a less favorable lipid profile (7, 8, 10, 17, 18, 19). However, to our knowledge, ours is the first study to assess differences in lipid metabolism in SGA newborns, including preterm infants, very early in life (3 d after delivery). The underlying mechanism linking SGA with adverse lipid levels is not well understood. It is generally assumed that factors influencing insulin sensitivity may explain the association between birth weight and dyslipidemia (10, 20, 21). Hyperinsulinemia is known to enhance hepatic very-low-density lipoprotein synthesis, which may contribute to increased plasma triglycerides and LDL-c levels (21, 22, 23, 24, 25). Resistance to the action of insulin on lipoprotein lipase in peripheral tissues may also contribute to elevated triglyceride and LDL-c levels (26). The present results indicated that further research is required to study lipids clearance in larger group of SGA infants in early postnatal period. We also found that the levels of serum triglycerides in all infants in our study were higher than what has been reported in other studies (7, 8). These findings may be a result of the enteral feeding, and probably represent lower total plasma lipoprotein lipase activity in newborn infants (27, 28).

We found no correlations between only premature births and any of the measured metabolic variables, which suggest that prematurity is less detrimental if neonates are AGA. This finding contrasts with the recent report of Hofman and colleagues (29), who observed a similar reduction in insulin sensitivity among both AGA and SGA former premature infants at 4 to 10 yr of age. The differences we observed in our study may be caused by the age groups of children in our study, in whom glucose and lipid metabolism were studied soon after birth, reducing the potential confounding effect of postnatal factors.

This study is limited by the lack of long-term metabolic data from these infants, but suggests that in the early postnatal period, SGA neonates show a trend toward lower insulin sensitivity and a less favorable lipid profile compared with AGA neonates. The long-term implications of the findings of this study are not yet known, including the duration of the metabolic differences found in our study.


   Acknowledgments
 
The authors thank Dr. Jacqueline Gindler (National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention) for proofreading the English.


   Footnotes
 
First Published Online December 5, 2006

Abbreviations: AGA, Appropriate for gestational age; LDL-c, low-density lipoprotein cholesterol; SGA, small for gestational age.

Received June 16, 2006.

Accepted November 22, 2006.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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