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Prevalence of Impaired Fasting Glucose and Its Relationship With Cardiovascular Disease Risk Factors in US Adolescents, 1999–2000

Desmond E. Williams, MD^*, Betsy L. Cadwell, MSPH^*, Yiling J. Cheng, PhD^*, Catherine C. Cowie, PhD, Edward W. Gregg, PhD^*, Linda S. Geiss, MA^*, Michael M. Engelgau, MD^*, K. M. Venkat Narayan, MD^* and Giuseppina Imperatore, MD^*

^* Division of Diabetes Translation, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland

	ABSTRACT

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Objective. PEDIATRICS (ISSN 0031 4005). Published in the public domain by the American Academy of Pediatrics.Several studies have reported increases in the occurrence of type 2 diabetes in youths. People with prediabetic states such as impaired fasting glucose (IFG) are at increased risk for developing diabetes and cardiovascular disease (CVD). The objective of this study was to examine the prevalence of IFG and its relationship with overweight and CVD risk factors in a nationally representative sample of US adolescents who were aged 12 to 19 years.

Methods. We used data from the 1999–2000 National Health and Nutrition Examination Survey (NHANES). Adolescents who had fasted for 8 hours or more were included in the study (n = 915). IFG was defined as a fasting glucose of 100 to 125 mg/dL. Participants were classified as overweight when their age- and gender-specific BMI was 95th percentile and as at-risk for overweight when their BMI was 85th and <95th percentile.

Results. In 1999–2000, the prevalence of IFG in US adolescents was 7.0% and was higher in boys than in girls (10.0% vs 4.0%). Prevalence of IFG was higher in overweight adolescents (17.8%) but was similar in those with normal weight and those who were at risk for overweight (5.4% vs 2.8%). The prevalence of IFG was significantly different across racial/ethnic groups (13.0%, 4.2%, and 7% in Mexican Americans, non-Hispanic black individuals, and non-Hispanic white individuals, respectively). Adolescents with IFG had significantly higher mean hemoglobin A1c, fasting insulin, total and low-density lipoprotein cholesterol, triglycerides, and systolic blood pressure and lower high-density lipoprotein cholesterol than those with normal fasting glucose concentrations.

Conclusions. These data, representing 27 million US adolescents, reveal a very high prevalence of IFG (1 in 10 boys and 1 in 25 girls) among adolescents; the condition affects 1 in every 6 overweight adolescents. Adolescents with IFG have features of insulin resistance and worsened CVD risk factors. Evidence for prevention is still forthcoming in this age group.

Key Words: children and adolescents • hyperglycemia • obesity • prevalence • survey

Abbreviations: ADA, American Diabetes Association • IFG, impaired fasting glucose • IGT, impaired glucose tolerance • CVD, cardiovascular disease • NHANES, National Health and Nutrition Examination Survey • FPG, fasting plasma glucose • HbA_1c, hemoglobin A1c • CI, confidence interval

In both 1997 and 2004, experts who were assembled by the American Diabetes Association (ADA) identified people with prediabetes, defined as impaired fasting glucose (IFG) or impaired glucose tolerance (IGT), as a high-risk group for the development of diabetes^1–3 and cardiovascular diseases (CVDs). Randomized, controlled trials involving adults with IGT, some of whom had IFG also, have provided strong evidence that lifestyle changes that include increased physical activity and dietary changes or metformin can significantly reduce the incidence of diabetes.^4–6 Such evidence has led the ADA to recommend diabetes prevention activities, such as lifestyle changes, for adults with prediabetic states. For children and adolescents, however, little is known about the prevalence of prediabetes and especially about IFG, the definition of which was revised recently. Likewise, the risk in children and adolescents with prediabetes for developing diabetes and CVD is unknown.

In this study, we examined the prevalence of IFG in a nationally representative sample of US adolescents who were aged 12 to 19 years. We also investigated the relationship between IFG and overweight and CVD factors.

	METHODS

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Study Design and Sample
Using a stratified, multistage probability sampling design, we examined data from the 1999–2000 National Health and Nutrition Examination Survey (NHANES 1999–2000), a nationally representative sample of the civilian, noninstitutionalized US population. NHANES 1999–2000 includes an oversampling of adolescents aged 12 to 19 years, black individuals, and Mexican Americans, as well as other groups. The survey received human subject review and approval. All participants signed informed consent documents. A total of 2309 adolescents were interviewed. Included in this analysis were 915 nonpregnant adolescent participants who did not have self-reported diabetes, who had fasted for 8 to 24 hours, and who had a valid fasting plasma glucose (FPG) measurement. Because these participants did not receive an oral glucose tolerance test, we were not able to estimate the prevalence of IGT and thus could not determine the total prevalence of prediabetes.

Measures and Data Collection
Participants were interviewed in their homes by trained bilingual interviewers using a computer-assisted interviewing system. After completing the interview, participants were invited to visit a specially equipped mobile examination center for the health examination component. The standardized examination included barefoot standing height (with a stadiometer), weight with minimal clothing (on a digital, electronic scale), and waist circumference (in the horizontal plane at a point marked just above the right ilium on the midaxillary line, at minimal respiration).⁷ Heights and circumferences were recorded to the nearest 0.1 cm.

The laboratory methods used at the mobile examination center have been reported in detail in the NHANES Laboratory/Medical Technologists Procedures Manual.⁸ In brief, blood samples were collected, processed, stored at –20°C, and shipped to the laboratory for analysis.⁹ FPG was measured by a modified hexokinase enzymatic method.⁹ Hemoglobin A1c (HbA_1c) was measured with the use of an automated high-performance liquid chromatography analyzer (Primus CLC330 and Primus CLC385, Primus Corporation Glycated Hemoglobin and Plasma Protein Analyzer; Primus Corp, Kansas City, MO) in accordance with the principles of boronate affinity.^10,11 Total cholesterol was measured enzymatically at the Johns Hopkins University Lipid Research Clinic Laboratory.¹² High-density lipoprotein cholesterol was measured in supernatants after precipitation of apo B–containing lipoproteins with heparin-manganese chloride and removal of excess manganese by precipitation with sodium bicarbonate.¹³ Friedewald's equation¹⁴ was used to calculate low-density lipoprotein cholesterol levels for participants with triglyceride levels of 400 mg/dL (4.52 mmol/L) or less. Triglycerides were analyzed enzymatically with the use of commercially available reagents. The overall interview and examination response rate among all of the participants in the survey was 82% and 76%, respectively.¹⁵

Definition of IFG
IFG was defined according to the 2004 ADA definition² as FPG of 100 mg/dL (5.6 mmol/L) to 125 mg/dL (7.0 mmol/L).

Data Analysis
Statistical analyses used SAS (Version 8.02; SAS Institute Inc, Cary, NC) for data management and SUDAAN (Version 8.0; Research Triangle Institute, Research Triangle Park, NC) to calculate standard errors, with the delete 1 jackknife method to account for the complex survey design. Sample weights to account for the probability of being sampled and adjusted for noncoverage and nonresponse were used in all analyses. Prevalence of IFG was based on those who were in the morning subsample and did not have diabetes; this is virtually the same as the prevalence of IFG in the total US population because the prevalence of diagnosed diabetes is so low (0.25%)¹⁶ in this age group.

BMI was calculated by dividing weight (in kilograms) by the square of the height (in meters). Participants were classified as overweight or at risk for overweight when their age- and gender-specific BMI was equal or above the 95th and 85th percentiles, respectively.^17,18 These BMI percentiles were calculated from a historic data set that contains data from 5 national surveys that were conducted between 1963 and 1994.¹⁸ Waist-to-height ratio was dichotomized at or above the gender-specific 95th percentile and used to examine the relationship between IFG and central obesity. The prevalence of IFG was examined by race/ethnicity, BMI, and waist-to-height categories. Significant differences in means were determined by t tests, and differences in proportions were tested using logistic regression models. When adjusting for covariates, we used predictive margins to estimate the probability of IFG.¹⁹ Estimates of the geometric mean (95% confidence interval [CI]) are presented for fasting insulin and triglyceride concentrations as the distributions of these variables were highly skewed.

	RESULTS

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Population Characteristics
The study population included 471 boys and 444 girls, representing 27 million US adolescents, with a mean age of 15.3 years (Table 1). In this sample, 16.1% were overweight (BMI 95th percentile) and an additional 13.9% were at risk of overweight (BMI 85th percentile and <95th percentile). The prevalence of overweight adolescents among non-Hispanic black individuals (23.9%; P < .02) and Mexican Americans (23.5%; P < .01) was significantly higher than that among non-Hispanic white individuals (11.9%). The proportion of adolescents with gender-specific waist-to-height ratio 95th percentile was also higher among non-Hispanic black individuals and Mexican Americans than non-Hispanic white individuals, but these differences were not significant (P > .05). Non-Hispanic black individuals had statistically significantly lower fasting glucose concentrations (P < .02) and higher HbA_1c (P < .001) than their non-Hispanic white and Mexican American counterparts.

Race/Ethnicity and IFG
The prevalence of IFG varied between the different racial/ethnic groups. The prevalence of IFG was significantly higher in Mexican Americans than in non-Hispanic black individuals (13.0% vs 4.2%; P < 0.01) even after adjustment for age, gender, and BMI (Table 2). Mexican American adolescents also had a higher prevalence of IFG than non-Hispanic white individuals (13.0% vs 7.0%), but this difference was not significant after adjustment for age, gender, and BMI. The prevalence of IFG in non-Hispanic white individuals was higher than but not significantly different from the prevalence in non-Hispanic black individuals (P > 0.05).

IFG and Cardiovascular Risk Factors
Adolescents with IFG had significantly higher HbA_1c, total and low-density lipoprotein cholesterol, fasting triglycerides, systolic blood pressure, and fasting insulin and lower high-density lipoprotein cholesterol than adolescents with normal fasting glucose (Table 3). Mean diastolic blood pressure in adolescents with IFG was not significantly different from that of adolescents with normal fasting glucose.

	DISCUSSION

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IFG was more prevalent in boys than in girls, although this difference was not statistically significant. The finding is consistent with several studies of adult populations showing IFG to be more common in men and IGT to be more common in women. Because we could not assess IGT in our study, we were unable to determine whether the same gender-specific differences apply to adolescents.

IFG is often a transient state, and our study thus is limited by the single measurement of FPG. FPG in adults is subject to significant intraindividual variation of up to 4.6% to 15%.^21,22 In adolescents, at different stages of puberty, the variations in FPG may be greater because of the marked influence of growth hormone on insulin resistance and glucose metabolism. One of the limitations of our study is the lack of direct measurement of puberty. Such detailed measurements are not usually available in nationally representative surveys, such as NHANES. Furthermore, the purpose of this article is to examine the prevalence of IFG in children and young adults and not to elucidate the role of contributing factors such as puberty. However, using a crude measure (age) of puberty, we found no evidence of an effect of puberty. More accurate methods of assessing puberty are needed to understand better its effect on the prevalence of IFG.

An unexpected finding was the lower mean fasting glucose concentration in black individuals as compared with the non-Hispanic white individuals, although black individuals had a higher degree of obesity and HbA_1c. We speculate that this finding may be explained by differences in the onset of puberty in these 2 populations and differences in intraindividual variability of fasting glucose.²³ The discordant results between HbA_1c and fasting glucose may reflect the low variance (2%–30%) in HbA_1c explained by fasting glucose within the normal range.²⁴ The remainder of the variance of HbA_1c may be explained by other factors, such as differences in red blood cell survival and the rate of glycation.^24,25

The ADA initially defined the lower limit for IFG as an FPG of 110 mg/dL¹ but lowered this to 100 mg/dL in early 2004.² This change in the definition of IFG, which has huge public health implications, resulted in an increase from 0.8% to 7.0%, an 8-fold increase (data not tabulated) in the prevalence of IFG among US adolescents. In adults aged 45 to 74 years, the prevalence of IFG increased almost 4-fold (from 8.3% to 30.2%) with the changed definition.²⁶

Little information is available about the progression of IFG to type 2 diabetes in adolescents. In adults, however, IFG is a risk factor for the development of diabetes. An International Diabetes Federation consensus workshop³ on IFG and IGT in adults concluded that >60% of people who developed diabetes had either IGT or IFG (defined at the time as FPG 110 and <126 mg/dL) within the 5-year period that preceded the diagnosis of diabetes.³ Similarly, IFG was identified as an independent risk factor for the development of diabetes in Finnish and Dutch adults.^27,28 In the Dutch study, 38% of Dutch adults with IFG and 32.4% with IGT developed diabetes over a 6-year period.²⁷ Studies on the progression of IFG in children and adolescents are needed to examine the long-term risks for developing both type 2 diabetes and CVD in this population.

The elevated risk for progression to type 2 diabetes in adults with fasting glucose between 95 and 125 mg/dL and with IGT, another prediabetic state, can be minimized by intensive lifestyle interventions that include physical activity and dietary changes.^4–6 Although not yet proved, it is likely that adolescents with prediabetes may also be able to reduce their future risk for diabetes and, hopefully, CVD by adopting these lifestyle interventions. Intervention studies such as the Studies to Treat or Prevent Pediatric Type 2 Diabetes²⁹ are testing the effectiveness of lifestyle interventions, at both institutional and individual levels, in reducing the risk for progression to type 2 diabetes in this age group.

IFG also identifies a high-risk group of adolescents who are more insulin resistant and have a more adverse lipid profile and higher systolic blood pressures, all of which have been shown to increase the development of atherosclerotic plaques in young adults. This result is not entirely surprising as the cardiovascular risk that occurs concomitantly with higher FPG is a continuum with no evidence of a threshold value.³⁰ The risk for development of CVD in children with prediabetes is unknown. However, the development of early indicators of CVD, such as atherosclerotic plaques³¹ and carotid intima-media thickness,^32–34 have been shown to begin in childhood and adolescence. The development of these early indicators of CVD has been related to hypertension, obesity, hypercholesterolemia, and hyperglycemia in children and adolescents in cross-sectional autopsy studies and cohort studies in Muscatine, Iowa,³² and Bogalusa, Louisiana.³³

We found a very high prevalence of IFG in US adolescents, 1 in 14 children aged 12 to 19. This translates to 2 million US children with IFG and many already showing signs of insulin resistance and worsened CVD risk factors. When left unchecked, the high prevalence of IFG in adolescents may foretell future increases in the incidence of diabetes. These data provide a baseline for monitoring national trends and also urge the need for diabetes prevention studies among adolescents.

	FOOTNOTES

 
Accepted Feb 4, 2005.

Reprint requests to (D.E.W.) Division of Diabetes Translation, NCCDPHP, Centers for Disease Control and Prevention, 4770 Buford Hwy, NE (MS-K10), Atlanta, GA 30341-3724. E-mail: dewilliams{at}cdc.gov

No conflict of interest declared.

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This Article Abstract Full Text (PDF) P3Rs: Submit a response Alert me when this article is cited Alert me when P3Rs are posted Alert me if a correction is posted Citation Map Services E-mail this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My File Cabinet Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via ISI Web of Science (17) Citing Articles via Google Scholar Google Scholar Articles by Williams, D. E. Articles by Imperatore, G. Search for Related Content PubMed PubMed Citation Articles by Williams, D. E. Articles by Imperatore, G. Related Collections Endocrinology

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