Published online November 1, 2005
PEDIATRICS Vol. 116 No. 5 November 2005, pp. 1178-1182 (doi:10.1542/peds.2004-2358)
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Development of the Metabolic Syndrome in Black and White Adolescent Girls: A Longitudinal Assessment

John A. Morrison, PhD*, Lisa Aronson Friedman, ScM{ddagger}, William R. Harlan, MD§, Linda C. Harlan, PhD||, Bruce A. Barton, PhD{ddagger}, George B. Schreiber, DSc and David J. Klein, MD, PhD#

Department of Pediatrics, University of Cincinnati Medical Center and the Divisions of * Cardiology
# Endocrinology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
{ddagger} Maryland Medical Research Institute, Baltimore, Maryland
§ National Institute of Mental Health
|| National Cancer Institute, Bethesda, Maryland
Westat, Rockville, Maryland


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background. The metabolic syndrome, associated with increased risk of type 2 diabetes mellitus and cardiovascular disease, begins to develop during adolescence.

Objective. We sought to identify early predictors of the presence of the syndrome at the ages of 18 and 19 years in black and white girls.

Methods. Using longitudinal data on participants from 2 centers in the National Heart, Lung, and Blood Institute Growth and Health Study, a 10-year cohort study, we applied cutoffs from the Adult Treatment Panel III to document changes in the prevalence of abnormal syndrome elements and the syndrome in girls aged 9 and 10 years, when cases were rare, and those aged 18 and 19 years, when prevalence had reached 3%. Longitudinal regression models identified early predictors for the presence of the syndrome.

Results. Only 1 girl of each race had ≥3 factors at ages 9 and 10 (0.2%), but 20 black girls (3.5%) and 12 white girls (2.3%) had the syndrome 10 years later. Low high-density lipoprotein cholesterol was prevalent throughout the period in both black and white girls. The prevalence of other variables was low at enrollment but increased during follow-up, except for abnormal triglyceride levels in black girls, which remained low throughout follow-up. In multivariate models, early measures of waist circumference and triglyceride level were significant predictors for development of the syndrome.

Conclusion. The strong association of central adiposity with the development of the metabolic syndrome suggests that early interventions aimed at managing preteen obesity could reduce risk of developing the syndrome.

Key Words: metabolic syndrome • adolescence • overweight • insulin resistance • ethnicity

Abbreviations: ATP III, Adult Treatment Panel III • HDL-C, high-density lipoprotein cholesterol • NHANES, National Health and Nutrition Examination Survey • NGHS, National Heart, Lung, and Blood Institute Growth and Health Study • HOMA-IR, homeostasis model assessment, insulin resistance

The metabolic syndrome, a constellation of factors including abdominal obesity, high blood pressure, dyslipidemias, and high fasting glucose levels, confers increased risk for diabetes mellitus and cardiovascular disease.1 The Adult Treatment Panel III (ATP III) defined the syndrome as the conjoint presence of ≥3 of the following factors: (1) a waist circumference ≥ 102 cm in men and 88 cm in women; (2) serum triglyceride level ≥ 150 mg/dL; (3) high-density lipoprotein cholesterol (HDL-C) level of ≤40 mg/dL in men and ≤50 mg/dL in women; (4) blood pressure ≥ 130/85 mm Hg; and (5) fasting glucose level ≥ 110 mg/dL.2 None of the cutoffs used to define these factors is extreme, representing instead the 80th to 85th percentiles of the factors as ascertained in epidemiologic surveys.3,4

Ford et al4 reported that ~22% of adults have the syndrome based on data from the representative sample of the US population in the National Health and Nutrition Examination Survey (NHANES) III. Other reports identified important roles for obesity and insulin resistance in the development of the syndrome.5–7 Cook et al8 reported on the prevalence of the syndrome phenotype in adolescents 12 to 19 years of age by using NHANES III data and redefining the cutoffs based on age-specific percentiles. This analytic strategy provided a sufficient number of cases to compare the prevalence across gender-race-ethnic groups but could not describe changes in the prevalence of the syndrome during adolescence because adjusted cutoffs were used. The Bogalusa Heart Study had begun before Kissebah et al9 identified central adiposity as a key predictor of metabolic disorders, but recent analyses of data from multiple Bogalusa surveys between 1978 and 1996, using BMI instead of waist circumference, showed that the clustered presence in childhood of top-quartile values for BMI, blood pressure, insulin level, and triglyceride level or low HDL-C levels predicted their clustered presence in young adulthood, ~11 years later.10 BMI and insulin were the strongest predictors in multiple logistic models, with BMI being the stronger of these 2.10

The dramatic rise in the prevalence of obesity in the years after NHANES II (1976–1980) and the attendant increase in the incidence of diabetes11 suggest that a prospective evaluation of the appearance of the syndrome during adolescence could provide insights into its pathogenesis and identify potential interventions. The National Heart, Lung, and Blood Institute Growth and Health Study12 (NGHS), a 10-year longitudinal study of adolescent obesity in black and white girls, provides an opportunity for such a prospective evaluation. Two NGHS clinical centers obtained fasting insulin and glucose measures at baseline and year 10 in addition to NGHS measures of anthropometry, lipids, and blood pressure.12 The purpose of this report is to identify early predictors of the syndrome's presence at ages 18 and 19 years. We hypothesized that early childhood obesity and fat distribution would predict the presence of the syndrome in early adulthood.


   METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The NGHS has been described in detail previously.12 Briefly, the study recruited 9- and 10-year-old girls in 1987–1988 who identified themselves as black or white, whose parents or guardians identified themselves as black or white, and who lived in racially concordant households. The Cincinnati, Ohio, and Washington, DC, clinics collected blood for the measurement of insulin and glucose at baseline and year 10 as part of an ancillary study. The institutional review boards at the 2 clinical sites approved the study, and signed, informed consent was obtained from the girls' parents or guardians.

Clinical and Laboratory Measures
Trained, certified staff took all clinical measures according to standard protocols.12 At annual visits, 2 measurements of height, weight, and, starting in year 2, the minimum waist circumference were made. A third measurement was taken if the first 2 differed by a preset amount. The mean of all measures was used in analyses. The BMI was used to evaluate overweight. Three blood pressure measurements were made at each visit by using a mercury sphygmomanometer and an appropriate-size cuff based on arm circumference.12 The mean of the second and third measurements of systolic or K-5 diastolic blood pressure was used in these analyses. Fasting HDL-C and triglyceride levels were measured by the Central Lipid Laboratory at Johns Hopkins University Medical Center (Baltimore, MD) at baseline and year 10,12 In years 1 and 10, plasma was obtained for insulin and glucose levels as reported previously.13 Homeostasis model assessment (HOMA-IR) was used as an index of insulin resistance.14

Statistical Analyses
The prevalence of abnormal levels of each component of the metabolic syndrome and the syndrome itself was calculated as the percent of participants with risk-factor values outside ATP III cutoffs. The use of age-specific 10th and 90th percentiles as cutoffs results in ~10% of participants with abnormal levels at both baseline and ages 18 and 19 years by design and, thus, could not demonstrate the emergence of the metabolic syndrome from being extremely rare or nonexistent to being a relatively common finding. When the ATP III cutoffs were used at year 10 only, the prevalence of high blood pressure and high triglyceride level was actually lower than at baseline by age-specific cutoffs. Because use of the ATP III cutoffs is appropriate at ages 18 and 19 years, these cutoffs were used at both visits, thus retaining a constant metric across the period and showing the appearance and development of the syndrome. General estimating equations were used to evaluate changes in the prevalence of individual syndrome components over time with race as an explanatory variable. Logistic-regression models were used to calculate the risk (odds ratios) of having the syndrome at ages 18 and 19 years that was associated with the presence of the elements that define the syndrome (waist circumference, glucose, triglycerides, HDL-C, and blood pressure) early in the study and with indices of obesity and insulin resistance, BMI, and HOMA-IR. All statistical analyses were performed with SAS 9.1.15


   RESULTS
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 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Table 1 presents baseline and year-10 descriptive data by race for the analysis cohort, including age, BMI, insulin, HOMA-IR, and the ATP III factors that define the metabolic syndrome. Black girls at baseline were slightly older (2 months) and had greater mean BMI, higher insulin, and higher HOMA-IR (all P < .0001) and higher HDL-C (P < .01) and glucose (P = .02) levels than white girls. As reported previously, multivariate analyses indicated that the differences in age and pubertal status did not explain the racial differences in obesity or insulin sensitivity.13 Black girls had higher systolic blood pressure (P = .01) and significantly lower triglyceride levels (P < .0001) at baseline. The measurement of waist circumference was begun in year 2; black girls had significantly larger mean waist circumference than white girls (P < .0001).


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  		TABLE 1. Age, BMI, Insulin, Glucose, HOMA-IR, Triglycerides, HDL-C, Systolic and Diastolic Blood Pressure, and Waist Circumference in Black and White Girls at Ages 9 and 10 and 18 and 19 Years According to Race and Age

 
As expected, there were significant increases in the means for BMI and the metabolic syndrome elements during follow-up, except for triglycerides, in black girls. The increases were 42.4% and 34.6%, respectively, for BMI in black and white girls and 20.3% and 18.8%, respectively, for waist circumference, thus amplifying baseline ethnic differences. Consistent with the increases in BMI and waist circumference, there were increases in mean systolic and diastolic blood pressure in both groups, but they were greater in black girls than white girls (systolic: P < .001; diastolic: P = .09) (Table 1). There was a significant increase in the mean triglyceride level in white girls (P < .001) but not in black girls. Decreases in the mean HDL-C level did not differ between groups. With completion of pubertal development, mean insulin level decreased in both groups; mean glucose level also decreased in both groups, but the decrease was greater in white girls (P = .02). Although HOMA-IR decreased in black girls and increased slightly in white girls, the absolute value remained lower in the white girls, indicating increased insulin resistance in black girls. Thus, at ages 18 and 19 years, black girls had significantly greater BMI, waist circumference, insulin level, HOMA-IR, and systolic blood pressure and lower triglyceride level (all P < .0001) and higher glucose level (P = .001) (Table 1). HDL-C level and diastolic blood pressure were also higher in black girls (P = .006). In addition to the changes in mean values during adolescence, there were significant increases in the dispersion of values for BMI and waist circumference in both groups and for triglyceride level in white girls, as shown by significantly larger variances (all P < .01). Thus, a larger percentage of girls had extreme (elevated) values for waist circumference and BMI and (white girls only) for triglycerides.

Table 2 presents the prevalence of the metabolic syndrome and its constituent factors at ages 9 and 10 and 18 and 19 years. As expected, the prevalence of the syndrome was low at baseline; at ages 9 and 10 years, only 1 girl (0.2%) in each racial group had ≥3 abnormal factors. The prevalence of abnormal factors was also low except for HDL-C, which had a prevalence of 37.3% in black girls and 40.6% in white girls. As a consequence of the increases in the mean and variances of anthropometric variables and the constituent factors discussed above, the prevalence of a large waist circumference and high blood pressure increased in both black and white girls (all P < .01). The prevalence of low HDL-C levels, already high in both groups at baseline, increased further. The prevalence of elevated triglyceride levels increased in white girls only (P < .01). The prevalence of an impaired fasting glucose level (≥110 mg/dL) increased little in either group. As a consequence of these changes, the prevalence of the syndrome at year 10 was 3.5% in black girls and 2.4% in white girls. Prevalence estimates for the syndrome were recalculated by using the new American Diabetic Association definition of an impaired fasting glucose level (≥100 mg/dL), which increased the prevalence of the syndrome from 20 to 21 (3.6%) in black girls and from 12 to 15 (3%) in white girls.


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  		TABLE 2. Prevalence of Metabolic Syndrome and Its Component Factors in Black and White Girls According to Visit (Age)

 
Early measures of the elements that define the syndrome plus BMI and HOMA-IR were all significant predictors of the development of the syndrome at ages 18 and 19 years in univariate logistic-regression models except for diastolic blood pressure (data not shown). When all these predictors were included in 1 multivariate model, multicollinearity was an issue. Therefore, separate models with BMI or waist circumference, race, and the other elements of the syndrome, 1 at a time, were used. As shown in Table 3, results indicated that BMI was significant in all models except when waist circumference was included, that waist circumference (P < .001) was significant in all models, that baseline triglyceride level was significant (P < .002) with either waist circumference or BMI in the model, and that HDL-C level was of borderline significance with BMI but not waist circumference. No other variable was significant when either BMI or waist circumference was in the model. For every increase of 1 cm in waist circumference at year 2, the risk of developing the syndrome increased 7.4%, and for every increase of 1 mg/dL in triglyceride level at baseline, the risk increased 1.3%. Race was not significant in any model.


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  		TABLE 3. Increased Risk of Metabolic Syndrome at Ages 18 and 19 Years From Multivariate Logistic-Regression Analysis Using Early Predictors, With BMI and Waist Circumference in the Models

 
To clarify the relationship between central adiposity in year 2 and the metabolic syndrome at ages 18 and 19 years, we examined the degree to which girls maintained their relative rank for waist circumference (ie, the degree to which waist circumference tracked from year 2 to 10). Adjusting for pubertal stage and race, the tracking coefficient was 0.83, indicating a very strong tendency for girls who had high central obesity in year 2 to continue having high central obesity through adolescence. Because a waist circumference of 72 cm in year 2 represented the same percentile in the distribution as a waist circumference of 88 cm in year 10, we compared the prevalence of the syndrome in girls with waist circumferences above these cutoffs at both years 2 and 10 and at year 2 only. There were 233 girls with a waist circumference ≥ 72 cm in year 2, 167 of which had a waist circumference ≥ 88 cm in year 10 and 66 of which did not. The prevalence of the metabolic syndrome in the 167 girls was 12.1% compared with 0% in the girls who had increased waist circumference at year 2 but not at year 10.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We report here the first large-scale, longitudinal assessment of the development of the metabolic syndrome during adolescence in girls by using the ATP III definition of the syndrome, a strategy that highlights the increase in prevalence during adolescence and factors related to it.

Although there was already 1 case in each group at baseline, we have shown the emergence of the syndrome during adolescence from (virtually) zero to a combined prevalence of 3% at young adulthood (3.4%, using the new American Diabetic Association definition of high glucose level). We have also identified the factors at years 1 and 2 that predict its presence 10 years later. The marked increase in the prevalence of the syndrome reflects increases in syndrome variables resulting (in part) from adolescent growth, but the increases in the dispersion of values for syndrome elements (larger variances) suggest that there is a subset of girls in whom the increases exceed normal growth.

Although the high prevalence of low HDL-C level in this sample is consistent with the NHANES III data in adult black and white women (34.0% and 39.3%, respectively4), the findings from this and the other studies raise questions about the appropriateness of this cutoff. Although the HDL-C cutoff of 40 mg/dL used in males is ~25th percentile, the cutoff of 50 mg/dL in women is closer to the 50th percentile and may identify too many cases of low HDL-C level. This issue needs to be reconsidered by the expert panels.

There were striking racial differences in the prevalence of individual components of the syndrome. The adolescent increases in body size and central adiposity were greater in black than white girls, as were the associated increases in systolic and diastolic blood pressure. At the same time, the increase in insulin sensitivity, reflected in lower glucose levels and HOMA-IR scores, which normally occurs with completion of pubertal development,16,17 reduced the risk of the syndrome due to this factor. Finally, there was a striking increase in abnormal triglyceride levels in white girls but not in black girls, despite the greater increases in BMI and waist circumference in black girls and the strong association between obesity and triglyceride levels in both black and white girls.18 This difference is part of the continuing puzzle of racial differences in triglyceride metabolism. It could reflect more subcutaneous adiposity and less visceral adiposity in black girls19 or a greater prevalence of the polymorphism of the hepatic lipase gene associated with low triglyceride levels, as reported by Vega et al,20 or both. Consequently, the contribution of elevated triglyceride levels to the presence of the syndrome is less in black girls. Reflecting all the changes in these individual factors, the prevalence of the syndrome increased in both races to 3.5% in black girls and 2.4% in white girls at ages 18 and 19 years. These observed prevalence levels are consonant with the percentages of affected females reported by Ford et al4 and represent levels midway between the estimates for ages 9 and 10 years and for ages 20 to 29 years (6%).

The results of this study underscore the importance of early central adiposity in the development of the metabolic syndrome. BMI can serve as a surrogate variable if waist circumference is not available, as shown by its significant relation to the syndrome in multivariate models except when waist circumference was included. The data show that the prevalence of the syndrome, which was 3% overall at ages 18 and 19 years, was 12.1% in the girls with persistently increased central adiposity and 0% in the girls who had increased waist circumference at year 2 but not at year 10. The tracking coefficient for waist circumference was high (82.3%), and ~72% of girls with increased central adiposity at ages 10 and 11 years by age-specific cutoffs had increased central adiposity at 18 and 19 years according to ATP III standards. These findings are consistent with earlier reports that waist circumference is the primary predictor of the metabolic consequences of obesity9,2122–23 and extend these findings by showing that what happens in childhood central adiposity is critical.

Strengths of the current report include its prospective design, relatively large sample size, and careful, collaborative protocol. Weaknesses of the report include the fact that the NGHS was designed to understand factors associated with racial differences in obesity and not to address questions concerning the evolution of insulin resistance, metabolic syndrome, and diabetes; hence, girls could participate in the NGHS without having blood drawn. Although participants with and without laboratory measures did not have mean BMI significantly different at baseline or in black girls in year 10, white girls who had blood drawn at ages 18 and 19 years had significantly lower mean BMI than those who did not. This could have affected prevalence estimates of elevated glucose and triglyceride levels and of the syndrome in white girls.

The development of abnormal levels of the individual elements constituting the metabolic syndrome can have its origins and onset in adolescence and develop through adulthood. Although very rare in prepuberty when adult standards are used, the components of the syndrome become increasingly common during adolescence, and the constellation of ≥3 components occurs in 3% of young adult women. The early predictors of metabolic syndrome can be identified before the complete syndrome is seen. Early recognition of central adiposity is critical, and as this study illustrates, preadolescent central adiposity that does not persist is not associated with increased incidence of the syndrome. Thus, taking action in adolescence could provide major health benefits.


   ACKNOWLEDGMENTS
 
This research was supported in part by National Institutes of Health, National Heart, Lung, and Blood Institute contracts HC-55023-26, HL 48941, and MO1 RR 08084


   FOOTNOTES
 
Accepted Jan 24, 2005.

Address correspondence to John A. Morrison, PhD, Division of Cardiology, Children's Hospital Medical Center, OSB 4, 3333 Burnet Ave, Cincinnati, OH 45229. E-mail: john.morrison{at}cchmc.org

No conflict of interest declared.


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Isomaa B, Almgren P, Tuomi T, et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 2001;24 :683 –689[Abstract/Free Full Text]
  2. Expert Panel on Detection, Evaluation, and Treatment of High Cholesterol in Adults. Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA. 2001;285 :2486 –2497[Free Full Text]
  3. US Department of Health and Human Services. The Lipid Research Clinics Population Studies Data Book. Vol I: The Prevalence Study. Bethesda, MD: US Department of Health and Human Services, Public Health Service: 1980. National Institutes of Health publication 80–1527
  4. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: findings from the Third National Health Examination Survey. JAMA. 2002;287 :356 –359[Abstract/Free Full Text]
  5. Haffner SM, Valdez RA, Hazuda HP, Mitchell BD, Morales PA, Stern MP. Prospective analysis of the incidence of the insulin-resistance syndrome (syndrome X). Diabetes. 1992;41 :715 –722[Abstract]
  6. Liese AD, Mayer-Davis EJ, Tyroler HA, et al. Development of the multiple metabolic syndrome in the ARIC cohort: joint contribution of insulin, BMI, and WHR: atherosclerosis risk in communities. Ann Epidemiol. 1997;7 :407 –416[CrossRef][ISI][Medline]
  7. Schmidt MI, Duncan BB, Watson RL, Sharrett AR, Brancati FL, Heiss G. A metabolic syndrome in whites and African Americans: the Atherosclerosis Risk in Communities Study. Diabetes Care. 1996;19 :414 –418[Abstract]
  8. Cook S, Weitzman M, Auinger P, Nguyen M, Dietz WH. Prevalence of metabolic syndrome phenotype in adolescents: findings from the Third National Health and Nutrition Examination Survey, 1988–1994. Arch Pediatr Adolesc Med. 2003;157 :821 –827[Abstract/Free Full Text]
  9. Kissebah AH, Vydelingum N, Murray R, et al. Relation of body fat distribution to metabolic complications of obesity. J Clin Endocrinol Metab. 1982;54 :254 –260[Abstract]
  10. Srinivasan SR, Myers L, Berenson GS. Predictibility of childhood adiposity and insulin for developing insulin resistance syndrome (syndrome X) in young adulthood: the Bogalusa Heart Study. Diabetes. 2002;51 :204 –209[Abstract/Free Full Text]
  11. Pinhas-Hamiel O, Dolan LM, Daniels SR, Standiford D, Khoury PR, Zeitler P. Increased incidence of non-insulin-dependent diabetes mellitus among adolescents. J Pediatr. 1996;128 :608 –615[CrossRef][ISI][Medline]
  12. The NHLBI Growth and Health Study Research Group. Obesity and cardiovascular disease risk factors in 9-and 10-year-old black and white girls: the NHLBI Growth and Health Study. Am J Public Health. 1992;82 :1613 –1620[Abstract/Free Full Text]
  13. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28 :412 –419[CrossRef][ISI][Medline]
  14. SAS Institute. SAS/STAT User's Guide. Version 8. Cary, NC: SAS Institute, Inc; 1999
  15. Klein DJ, Aronson Friedman L, Harlan WR, et al. Obesity and the development of insulin resistance and impaired fasting glucose in black and white adolescent girls: a longitudinal study. Diabetes Care. 2004;27 :378 –383[Abstract/Free Full Text]
  16. Kuczmarski RJ, Ogden CL, Guo SS, et al. 2000 CDC growth charts for the United States: methods and development. National Center for Healh Statistics. Vital Health Stat 11. 2002;(246):1–190
  17. Moran A, Jacobs DR Jr, Steinberger J, et al. Insulin resistance during puberty: results from clamp studies in 357 children. Diabetes. 1999;48 :2039 –2044[Abstract]
  18. Morrison JA, McMahon RP, Sprecher DL, Simon JA. Obesity and high-density lipoprotein cholesterol in black and white 9- and 10-year-old girls: the National Heart, Lung, and Blood Institute Growth and Health Study. Metabolism. 1996;45 :469 –475[CrossRef][ISI][Medline]
  19. Morrison JA, Barton BA, Obarzanek E, et al. Racial differences in sums of skinfolds and percent body fat estimated from impedance in black and white girls, 9–19 years of age: the NHLBI Growth and Health Study [published correction appears in Obes Res. 2001;9:510]. Obes Res. 2001;9 :297 –305[ISI][Medline]
  20. Vega GL, Clark LT, Tang A, Marcovina S, Grundy SM, Cohen JC. Hepatic lipase is lower in African American men than in white American men: effects of 5' flanking polymorphism in the hepatic lipase gene (LIPC). J Lipid Res. 1998;39 :228 –232[Abstract/Free Full Text]
  21. Hartz AJ, Rupley DC, Rimm AA. The association of girth measurements with disease in 32,856 women. Am J Epidemiol. 1984;119 :71 –80[Abstract/Free Full Text]
  22. Stevens J, Keil JE, Rust PF, Tyroler HA, Davis CE, Gazes PC. Body mass index and body girths as predictors of mortality in black and white women. Arch Intern Med. 1992;152 :1257 –1262[Abstract]
  23. Bjorntorp P. Body fat distribution, insulin resistance, and metabolic diseases. Nutrition. 1997;13 :795 –803[CrossRef][ISI][Medline]
PEDIATRICS (ISSN 1098-4275). ©2005 by the American Academy of Pediatrics



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