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Diabetes Care 29:781-785, 2006
DOI: 10.2337/diacare.29.04.06.dc05-1523
© 2006 by the American Diabetes Association
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Clinical Care/Education/Nutrition
Original Article

Low–Saturated Fat Dietary Counseling Starting in Infancy Improves Insulin Sensitivity in 9-Year-Old Healthy Children

The Special Turku Coronary Risk Factor Intervention Project for Children (STRIP) study

Tuuli Kaitosaari, MD1, Tapani Rönnemaa, MD, PHD2, Jorma Viikari, MD, PHD2, Olli Raitakari, MD, PHD3, Martti Arffman, MSC1, Jukka Marniemi, PHD4, Katariina Kallio, MD1, Katja Pahkala, MSC1, Eero Jokinen, MD, PHD5 and Olli Simell, MD, PHD6

1 Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, Turku, Finland
2 Department of Medicine, University of Turku, Turku, Finland
3 Clinical Physiology, Turku, Finland
4 National Public Health Institute, Turku, Finland
5 Hospital for Children and Adolescents, Helsinki, Finland
6 Department of Pediatrics, University of Turku, Turku, Finland

Address correspondence and reprint requests to Tuuli Kaitosaari, MD, Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, Kiinamyllynkatu 10, FIN-20520 Turku, Finland. E-mail: tuuli.kaitosaari{at}utu.fi


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
OBJECTIVE—Insulin resistance is promoted already in childhood by obesity and possibly by high–saturated fat intake. We examined the effect of infancy onset biannually given dietary counseling on markers of insulin resistance in healthy 9-year-old children.

RESEARCH DESIGN AND METHODS—Healthy 7-month-old infants (n = 1,062) were randomized to the intervention (n = 540) and control (n = 522) groups. Each year, two individualized counseling sessions were organized to each intervention family. The purpose of counseling was to minimize children’s exposure to known environmental atherosclerosis risk factors. Homeostasis model assessment of insulin resistance (HOMA-IR) index, serum lipids, blood pressure, and weight for height were determined in a random subgroup of 78 intervention children and 89 control children at the age of 9 years.

RESULTS—Intervention children consumed less total and saturated fat than the control children (P = 0.002 and < 0.0001, respectively). The HOMA-IR index was lower in intervention children than in control children (P = 0.020). There was a significant association between saturated fat intake and HOMA-IR. In multivariate analyses including saturated fat intake, study group, and other determinants of HOMA-IR (serum triglyceride concentration, weight for height, and systolic blood pressure), study group was, whereas saturated fat intake was not, significantly associated with HOMA-IR. This suggests that the beneficial effect of intervention on insulin sensitivity was largely, but not fully, explained by the decrease in saturated fat intake.

CONCLUSIONS—The long-term biannual dietary intervention decreases the intake of total and saturated fat and has a positive effect on insulin resistance index in 9-year-old children.

Abbreviations: apo, apolipoprotein • HOMA-IR, homeostasis model assessment of insulin resistance • PAI-1, plasminogen activator inhibitor type 1 • STRIP, Special Turku Coronary Risk Factor Intervention Project for Children


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
Insulin resistance, defined as an inadequate metabolic response to plasma insulin at normal concentrations (1,2), is promoted by obesity and high intake of saturated fat (3–5), and up to 30% of overweight or obese individuals develop insulin resistance (6). Although the prevalence of the insulin resistance syndrome, i.e., a cluster of metabolic abnormalities associated with reduced insulin sensitivity, increases with age, it exists already in childhood (7,8). In adults, the insulin resistance syndrome is associated with type 2 diabetes and cardiovascular disease (1). Preventing obesity and sedentary lifestyle and supporting a healthy lifestyle are important preventive measures, particularly if started in childhood.

The aim of the present study was to evaluate the effect of individualized repeatedly given dietary counseling aimed at a low–saturated fat low-cholesterol diet from the age of 7 years on serum insulin values and some other markers of the insulin resistance syndrome in 9-year-old healthy children.


   RESEARCH DESIGN AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
RESULTS
 CONCLUSIONS
 References
 
The study design of the ongoing prospective randomized Special Turku Coronary Risk Factor Intervention Project for Children (STRIP) study, which began in 1990, has been published in detail (9,10). Briefly, 1,054 volunteer families with 1,062 healthy 7-month-old infants were recruited to the study by nurses at the well-baby clinics in the city of Turku, Finland. The children were randomized to an intervention group (n = 540, 284 boys) or a control group (n = 522, 266 boys). At the age of 7 years, a time-restricted subsample of 200 children from both intervention and control groups was taken for more detailed laboratory measurements. In practice, to this cohort, we took those consecutive children who came to their 7-year annual STRIP visit (50 intervention boys, 50 intervention girls, 50 control boys, and 50 control girls) beginning January 1997 and ending November 1997. Selection bias did not occur. The participants of this present study comprised all 167 children of those original 200 who had blood samples available from their 9-year STRIP visit (78 intervention children, 35 boys; 89 control children, 47 boys).

Twice a year, the intervention group received individualized dietary counseling given by a team consisting of a physician and a dietitian. The families recorded the child’s food consumption for four optional consecutive days, including at least one weekend day, close (within 3 weeks) to each follow-up visit (11). A dietitian checked the food records and suggested appropriate changes to the diet. From the beginning of the study, the intervention group was supported to adopt a healthy low–saturated fat low-cholesterol diet, which was designed to meet the Nordic Dietary Recommendations (12). Since the age of 3 years, the recommended intakes comprised protein 10–15 E% (percentage of energy), fat 30 E% (saturated fat ≤10 E%), and carbohydrate 55–60 E%.

The control children have received the basic health education given at the Finnish well-baby clinics. During their STRIP visits, they received no detailed dietary counseling.

The study was approved by the Joint Commission on Ethics of the Turku University and the Turku University Central Hospital. Informed consent was obtained from all parents.

Anthropometric measurements
Weight was measured with an electronic scale (S10; Soehnle, Murrhardt, Germany) to the nearest 0.1 kg. Standing height was measured with a wall-mounted stadiometer (Harpenden Stadiometer, Holtain, Crymych, U.K.) to the nearest 0.1 cm. Both measurements were taken in the fasting state, with the subject dressed in light clothing without shoes. The weight, weight for height (deviation of weight in percentages from the mean weight of healthy Finnish children of the same age, height, and sex), and height were recorded (13). Waist (midway between iliac crest and the lowest rib at the midaxillary line) and hip (maximum width over the greater trochanters) circumferences were measured with a flexible measuring tape to the nearest 0.5 cm. All children except 11 girls (4 intervention and 7 control girls) were prepubertal, i.e., at Tanner stage 1 (14). These 11 girls were all at Tanner stage 2, and none of them had had menarche.

Laboratory methods
Fasting serum total and HDL cholesterol, apolipoprotein (apo)A-1, apoB, and triglyceride concentrations were measured as described (10). The Friedewald formula (15) was used to calculate serum LDL cholesterol concentration. Blood samples for determination of serum glucose and insulin concentrations were obtained after an overnight fast. The samples were centrifuged immediately, and 15 µl of the enzyme inhibitor Antagosan was added to the 0.5-ml serum insulin sample. Samples were stored at –20°C for 2 months at the most. Serum glucose was measured by the glucose dehydrogenase method (Merck Diagnostica, Darmstadt, Germany) and serum insulin by radioimmunoassay (Pharmacia Diagnostics, Uppsala, Sweden). The intra-assay of insulin variations was 2.89% at the average concentration of 16.5 mU/l and 3.12% at the level of 142 mU/l. The interassay variations were 3.89 and 3.91%, respectively. Plasminogen activator inhibitor type 1 (PAI-1) was assessed by a chromogenic assay kit based on two-stage indirect enzymatic assay (Spectrolyse/PL PAI; Biopool International, Ventura, CA). The intra-assay variations were 2.8% at the concentration of 17.5 units/ml and 2.3% at the concentration of 28.7 units/ml. The interassay variations were 4.8 and 8.6%, respectively. The homeostasis model assessment of insulin resistance (HOMA-IR) method was used to estimate insulin resistance as described [(fasting insulin mU/ml x fasting glucose mmol/l)/22.5] (16). The analyses were performed in the laboratory of the Research and Development Unit of Social Insurance Institution (Turku, Finland).

Statistical analysis
Two-way ANOVA was used to compare the means of anthropometric measurements, serum lipid values, markers of insulin resistance, blood pressure, and dietary intakes between the intervention and control groups and between sexes.

ANCOVA was used to determine correlates of the HOMA-IR index. First, because of the interdependency between various anthropometric variables, between serum lipid values, between energy nutrient intakes, and between systolic and diastolic blood pressure, one variable within each of these four variable groups was selected for the ANCOVA analyses based on their known associations with insulin resistance (1,2,4,7). These selected variables were as follows: weight for height, serum triglyceride concentration, saturated fat intake, and systolic blood pressure.

Serum insulin and triglyceride concentrations, plasma PAI-1 concentration, HOMA-IR values, and weight and weight for height values were log-transformed for the analyses. The results are presented as means ± SD unless otherwise stated. In all tests, P ≤ 0.05 was considered significant. Statistical analyses were performed using SAS System for Windows, release 9.1.3 (SAS, Cary, NC).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
CONCLUSIONS
 References
 
Weight, height, weight for height, waist circumference, blood pressure, and intakes of monounsaturated fat and sucrose did not differ between groups or sexes (Table 1). Intakes of total and saturated fat were lower, and intake of polyunsaturated fat was higher in intervention children than in control children. Intake of carbohydrate was higher in the intervention group than in the control group, but the intervention effect was divergent in boys and girls (Table 1). Intervention girls had a higher intake of carbohydrate than control girls. Girls had greater hip circumference and lower intakes of total energy and polyunsaturated fat than boys.


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  		Table 1— Anthropometric variables, blood pressure, and energy nutrient intakes of intervention and control children

 
Serum glucose concentration was slightly higher and insulin concentration was clearly lower in intervention children than in control children (Table 2). Boys had higher glucose concentrations than girls, but their insulin and PAI-1 concentrations were lower than in girls. HOMA-IR was lower in intervention children than in control children and lower in boys than in girls. Serum total and LDL cholesterol and apoA-1 and apoB concentrations did not differ between groups. LDL and apoB concentrations were lower in boys than in girls. Serum HDL cholesterol concentration did not differ between groups but was higher in boys than in girls. Serum triglyceride concentration was lower in intervention children than in control children and lower in boys than in girls. The 11 girls who had reached Tanner stage 2 did not differ in their basic anthropometric variables, blood pressure, energy nutrient intakes, insulin resistance markers, or serum lipid variables from prepubertal girls, except that apoB concentration was slightly higher in pubertal girls (0.76 vs. 0.66 mmol/l, P = 0.043).


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  		Table 2— Serum glucose and insulin, plasma PAI-1, HOMA-IR, serum lipid values, and apolipoproteins in intervention and control children

 
We performed separate analyses to examine possible factors explaining insulin resistance in general and to determine the mechanisms of how intervention leads to decreased insulin resistance. Study group, sex, saturated fat intake, serum triglyceride concentration, weight for height, and systolic blood pressure were associated with HOMA-IR (Table 3). Saturated fat intake was associated strongly with the intervention group (P < 0.0001). We included saturated fat intake in the ANCOVA analyses including study group and other determinants of HOMA-IR to examine whether the effect of intervention is so strongly explained by reduced saturated fat intake that the difference between groups in HOMA-IR would disappear. However, in the final multivariate model including study group, saturated fat intake was no more significantly associated with HOMA-IR, whereas study group was still significantly related to HOMA-IR. In the final multivariate ANCOVA model, significant explanatory variables for the HOMA-IR index were study group, serum triglyceride concentration, weight for height, and systolic blood pressure. The effect of weight for height was stronger in intervention children than in control children and in girls than in boys (Table 3, final multivariate model).


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  		Table 3— Determinants of HOMA insulin resistance index in 167 healthy study children

 

   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
References
 
Insulin resistance, hypertriglyceridemia, elevated blood pressure, and obesity are closely related (1,17). The present study showed that repeatedly given dietary counseling with onset in infancy, aimed at permanently low intake of saturated fat, seems to improve insulin sensitivity in 9-year-old children. At the dietary intake level, intervention was effective because intervention children consumed less total and saturated fat and more carbohydrate and polyunsaturated fat than control children.

High intake of saturated fat seems to associate with insulin resistance (3,4,18). When saturated fatty acid intake is excessive, triglycerides accumulate in many tissues, e.g., in liver and muscle leading to cellular damage and dysfunction and eventually causing hyperinsulinemia to compensate for insulin resistance (19). In our study, high–saturated fat intake was a significant explanatory variable of HOMA-IR when children from both study groups were analyzed together. However, when study group was included as a covariate in the model, the significance of saturated fat intake disappeared. This indicates that our finding of decreased HOMA-IR in intervention children is to a large extent due to their lower saturated fat intake. However, as the study group remained as a significant determinant of HOMA-IR after multiple adjustments, other unmeasured factors, such as possible altered exercise habits, may partly explain our intervention effect on HOMA-IR. Hypertriglyceridemia increases the amount of free fatty acids, which are known to promote insulin resistance (20). In the KANWU Study (4), insulin sensitivity was significantly impaired after a 3-month consumption of a high–saturated fat diet, while it remained unchanged on a monounsaturated fatty acid diet. In the Finnish Diabetes Prevention Study, a 3-year individualized lifestyle intervention reduced the intake of both total and saturated fat, and as a consequence, the incidence of diabetes in these overweight originally nondiabetic adults diminished (21). In the present study, study group and serum triglyceride concentration were significant explanatory variables for HOMA-IR index in the multivariate ANCOVA model study group. This suggests that the observed difference in HOMA-IR between intervention and control groups, most probably due to reduced saturated fat intake in intervention children, cannot solely be explained by mechanisms related to higher triglyceride levels in control children.

Adiposity in childhood may be the strongest predictor of the metabolic syndrome in adulthood (22), and overweight children are at increased risk of becoming obese adults (23,24). In a previous study on Finnish children, fasting serum insulin concentrations correlated positively with BMI in 9-year-old boys and girls (25). In accordance with that and other previous studies (8,26–29), we also observed a strong connection between children’s body composition and HOMA-IR. It is highly likely that obesity and insulin resistance have adverse subclinical cardiovascular consequences already in childhood. According to autopsy studies, BMI relates to the existence of fibrous plaques and fatty streaks in coronary arteries and aorta already in young children (30,31). A noninvasive ultrasound study of 10-year-old children revealed that obese girls have increased stiffness of abdominal aorta (32). In the study by Raitakari et al. (33), BMI and blood pressure in childhood correlated positively with the intima-media thickness of the common carotid artery in adulthood.

In the present study, sex was not associated with the HOMA-IR index in the multivariate model including study group. However, boys had lower HOMA-IR as well as serum triglyceride, LDL cholesterol, and apoB concentrations than girls. Total and saturated fat intakes did not differ between sexes, but boys had higher polyunsaturated fat intake than girls. Physical exercise improves insulin sensitivity (34) and affects serum lipid values favorably (35). Unfortunately, the level of physical activity was not accurately measured in the present study. However, in another Finnish study, boys under 12 years of age were physically more active than girls (36). Thus, it is probable that boys in the present study were more active than girls, which may explain the more favorable lipid pattern and lower HOMA-IR index in boys.

In conclusion, the 9 years of biannual nutrition counseling aimed at diminished intake of saturated fat seems to protect children from the development of insulin resistance. Clear-cut explanatory factors for higher insulin resistance index were (in addition to belonging to the control group having high–saturated fat intake) body composition, serum triglyceride concentration, and systolic blood pressure. Our results, if sustained for future decades, thus suggest that development of insulin resistance and subsequently possibly also atherosclerosis may be delayed or prevented by introducing relevant dietary and lifestyle habits already in early childhood. Further follow-up studies with continuing counseling sessions in our trial will show whether the observed beneficial effects of intervention will continue over puberty into early adulthood.


   Acknowledgments
 
This study was supported by grants from the Juho Vainio Foundation; the Yrjö Jahnsson Foundation; the Finnish Cardiac Research Foundation; the Foundation for Pediatric Research, Finland; the Academy of Finland (grant number 73582); the Sigrid Juselius Foundation; the Turku University Foundation; the Finnish Cultural Foundation, City of Turku; EVO funds of Turku University Central Hospital; and the Raisio Group Research Foundation.


   Footnotes
 
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C Section 1734 solely to indicate this fact.

Received for publication August 15, 2005. Accepted for publication January 4, 2006.


   References
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 

  1. Reaven GM: Banting Lecture 1988: Role of insulin resistance in human disease. Diabetes 37:1595–1607, 1988[Abstract]
  2. Garg A: Insulin resistance in the pathogenesis of dyslipidemia. Diabetes Care 19:387–389, 1996[Medline]
  3. Mayer EJ, Newman B, Quesenberry CP Jr, Selby JV: Usual dietary fat intake and insulin concentrations in healthy women twins. Diabetes Care 16:1459–1469, 1993[Abstract]
  4. Vessby B, Uusitupa M, Hermansen K, Riccardi G, Rivellese AA, Tapsell LC, Nalsen C, Berglund L, Louheranta A, Rasmussen BM, Calvert GD, Maffetone A, Pedersen E, Gustafsson IB, Storlien LH: Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU Study. Diabetologia 44:312–319, 2001[Medline]
  5. Abate N, Garg A, Peshock RM, Stray-Gundersen J, Grundy SM: Relationships of generalized and regional adiposity to insulin sensitivity in men. J Clin Invest 96:88–98, 1995[Medline]
  6. Ford ES, Giles WH, Dietz WH: Prevalence of the metabolic syndrome among US adults: findings from the Third National Health and Nutrition Examination Survey. JAMA 287:356–359, 2002[Abstract/Free Full Text]
  7. Sinaiko AR, Jacobs DR Jr, Steinberger J, Moran A, Luepker R, Rocchini AP, Prineas RJ: Insulin resistance syndrome in childhood: associations of the euglycemic insulin clamp and fasting insulin with fatness and other risk factors. J Pediatr 139:700–707, 2001[Medline]
  8. Raitakari OT, Porkka KV, Rönnemaa T, Knip M, Uhari M, Åkerblom HK, Viikari JS: The role of insulin in clustering of serum lipids and blood pressure in children and adolescents: the Cardiovascular Risk in Young Finns Study. Diabetologia 38:1042–1050, 1995[Medline]
  9. Lapinleimu H, Viikari J, Jokinen E, Salo P, Routi T, Leino A, Rönnemaa T, Seppänen R, Välimäki I, Simell O: Prospective randomised trial in 1,062 infants of diet low in saturated fat and cholesterol. Lancet 345:471–476, 1995[Medline]
  10. Niinikoski H, Viikari J, Rönnemaa T, Lapinleimu H, Jokinen E, Salo P, Seppänen R, Leino A, Tuominen J, Välimäki I, Simell O: Prospective randomized trial of low-saturated-fat, low-cholesterol diet during the first 3 years of life: the STRIP baby project. Circulation 94:1386–1393, 1996[Abstract/Free Full Text]
  11. Talvia S, Lagström H, Räsänen M, Salminen M, Räsänen L, Salo P, Viikari J, Rönnemaa T, Jokinen E, Vahlberg T, Simell O: A randomized intervention since infancy to reduce intake of saturated fat: calorie (energy) and nutrient intakes up to the age of 10 years in the Special Turku Coronary Risk Factor Intervention Project. Arch Pediatr Adolesc Med 158:41–47, 2004[Abstract/Free Full Text]
  12. Nordic nutrition recommendations 1996: Nordic working group on diet and nutrition. Scand J Nutr 40:161–165, 1996
  13. Sorva R, Lankinen S, Tolppanen EM, Perheentupa J: Variation of growth in height and weight of children. II. After infancy. Acta Paediatr Scand 79:498–506, 1990[Medline]
  14. Tanner JM, Whitehouse RH: Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51:170–179, 1976[Abstract]
  15. Friedewald WT, Levy RI, Fredrickson DS: Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502, 1972[Abstract]
  16. 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 28:412–419, 1985[Medline]
  17. Grundy SM: Hypertriglyceridemia, atherogenic dyslipidemia, and the metabolic syndrome. Am J Cardiol 81:18B–25B, 1998[Medline]
  18. Virtanen SM, Aro A: Dietary factors in the aetiology of diabetes. Ann Med 26:469–478, 1994[Medline]
  19. Manco M, Calvani M, Mingrone G: Effects of dietary fatty acids on insulin sensitivity and secretion. Diabetes Obes Metab 6:402–413, 2004[Medline]
  20. Randle PJ, Garland PB, Hales CN, Newsholme EA: The glucose fatty-acid cycle: its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1:785–789, 1963[Medline]
  21. Lindström J, Louheranta A, Mannelin M, Rastas M, Salminen V, Eriksson J, Uusitupa M, Tuomilehto J: The Finnish Diabetes Prevention Study (DPS): lifestyle intervention and 3-year results on diet and physical activity. Diabetes Care 26:3230–3236, 2003[Abstract/Free Full Text]
  22. Srinivasan SR, Myers L, Berenson GS: Predictability of childhood adiposity and insulin for developing insulin resistance syndrome (syndrome X) in young adulthood: the Bogalusa Heart Study. Diabetes 51:204–209, 2002[Abstract/Free Full Text]
  23. Daniels SR, Arnett DK, Eckel RH, Gidding SS, Hayman LL, Kumanyika S, Robinson TN, Scott BJ, St Jeor S, Williams CL: Overweight in children and adolescents: pathophysiology, consequences, prevention, and treatment. Circulation 111:1999–2012, 2005[Abstract/Free Full Text]
  24. Freedman DS, Khan LK, Dietz WH, Srinivasan SR, Berenson GS: Relationship of childhood obesity to coronary heart disease risk factors in adulthood: the Bogalusa Heart Study. Pediatrics 108:712–718, 2001[Abstract/Free Full Text]
  25. Rönnemaa T, Knip M, Lautala P, Viikari J, Uhari M, Leino A, Kaprio EA, Salo MK, Dahl M, Nuutinen EM, et al.: Serum insulin and other cardiovascular risk indicators in children, adolescents and young adults. Ann Med 23:67–72, 1991[Medline]
  26. Travers SH, Jeffers BW, Bloch CA, Hill JO, Eckel RH: Gender and Tanner stage differences in body composition and insulin sensitivity in early pubertal children. J Clin Endocrinol Metab 80:172–178, 1995[Abstract]
  27. Moran A, Jacobs DR Jr, Steinberger J, Hong CP, Prineas R, Luepker R, Sinaiko AR: Insulin resistance during puberty: results from clamp studies in 357 children. Diabetes 48:2039–2044, 1999[Abstract]
  28. Galli-Tsinopoulou A, Karamouzis M, Nousia-Arvanitakis S: Insulin resistance and hyperinsulinemia in prepubertal obese children. J Pediatr Endocrinol Metab 16:555–560, 2003[Medline]
  29. Reinehr T, Kiess W, Kapellen T, Andler W: Insulin sensitivity among obese children and adolescents, according to degree of weight loss. Pediatrics 114:1569–1573, 2004[Abstract/Free Full Text]
  30. Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA: Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults: the Bogalusa Heart Study. N Engl J Med 338:1650–1656, 1998[Abstract/Free Full Text]
  31. Kortelainen ML: Adiposity, cardiac size and precursors of coronary atherosclerosis in 5- to 15-year-old children: a retrospective study of 210 violent deaths. Int J Obes Relat Metab Disord 21:691–697, 1997[Medline]
  32. Iannuzzi A, Licenziati MR, Acampora C, Salvatore V, De Marco D, Mayer MC, De Michele M, Russo V: Preclinical changes in the mechanical properties of abdominal aorta in obese children. Metabolism 53:1243–1246, 2004[Medline]
  33. Raitakari OT, Juonala M, Kähönen M, Taittonen L, Laitinen T, Mäki-Torkko N, Järvisalo MJ, Uhari M, Jokinen E, Rönnemaa T, Åkerblom HK, Viikari JS: Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascular Risk in Young Finns Study. JAMA 290:2277–2283, 2003[Abstract/Free Full Text]
  34. Borghouts LB, Keizer HA: Exercise and insulin sensitivity: a review. Int J Sports Med 21:1–12, 2000[Medline]
  35. Raitakari OT, Taimela S, Porkka KV, Telama R, Välimäki I, Åkerblom HK, Viikari JS: Associations between physical activity and risk factors for coronary heart disease: the Cardiovascular Risk in Young Finns Study. Med Sci Sports Exerc 29:1055–1061, 1997[Medline]
  36. Telama R, Yang X: Decline of physical activity from youth to young adulthood in Finland. Med Sci Sports Exerc 32:1617–1622, 2000[Medline]

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