Correlation of Insulin Resistance with Anthropometric Measures and Blood Pressure in Adolescents

Abstract

Background:

Blood pressure is directly related to body mass index, and individuals with increased waist circumference have higher risk of developing hypertension, insulin resistance, and other metabolic changes, since adolescence.

Objective:

to evaluate the correlation of blood pressure with insulin resistance, waist circumference and body mass index in adolescents.

Methods:

Cross-section study on a representative sample of adolescent students. One group of adolescents with altered blood pressure detected by casual blood pressure and/or home blood pressure monitoring (blood pressure > 90^th percentile) and one group of normotensive adolescents were studied. Body mass index, waist circumference were measured, and fasting glucose and plasma insulin levels were determined, using the HOMA-IR index to identify insulin resistance.

Results:

A total of 162 adolescents (35 with normal blood pressure and 127 with altered blood pressure) were studied; 61% (n = 99) of them were boys and the mean age was 14.9 ± 1.62 years. Thirty-eight (23.5%) adolescents had altered HOMA-IR. The group with altered blood pressure had higher values of waist circumference, body mass index and HOMA-IR (p<0.05). Waist circumference was higher among boys in both groups (p<0.05) and girls with altered blood pressure had higher HOMA-IR than boys (p<0.05). There was a significant moderate correlation between body mass index and HOMA-IR in the group with altered blood pressure (ρ = 0.394; p < 0.001), and such correlation was stronger than in the normotensive group. There was also a significant moderate correlation between waist circumference and HOMA-IR in both groups (ρ = 0.345; p < 0.05). Logistic regression showed that HOMA-IR was as predictor of altered blood pressure (odds ratio - OR = 2.0; p = 0.001).

Conclusion:

There was a significant association of insulin resistance with blood pressure and the impact of insulin resistance on blood pressure since childhood. The correlation and association between markers of cardiovascular diseases was more pronounced in adolescents with altered blood pressure, suggesting that primary prevention strategies for cardiovascular risk factors should be early implemented in childhood and adolescence.

Keywords:
Blood Pressure; Body Mass Index; Insulin Resistance; Anthropometry; Adolescent

Resumo

Fundamentos:

A pressão arterial (PA) está diretamente relacionada com o índice de massa corporal (IMC), e indivíduos com circunferência da cintura (CC) aumentada apresentam risco maior de desenvolver hipertensão arterial e resistência à insulina, além de outras alterações metabólicas, desde a adolescência.

Objetivos:

Avaliar a correlação entre resistência à insulina, CC e IMC com PA de adolescentes.

Métodos:

Estudo transversal com amostra representativa de adolescentes escolares. Foram avaliados um grupo com PA alterada pela medida casual e/ou medida residencial da PA (percentil de PA > 90) e outro com PA normal. Foram também avaliados IMC e CC. Glicemia de jejum e insulina plasmática foram dosados utilizando o índice de HOMA-IR para resistência à insulina.

Resultados:

Foram estudados 162 adolescentes (35 no Grupo PA normal e 127 no Grupo PA alterada); 61,1% (n = 99) deles eram meninos, e a idade média foi 14,9 ± 1,62 anos. Foram observados 38 adolescentes (23,5%) com HOMA-IR alterado. Os adolescentes com PA alterada apresentaram valores maiores de CC, IMC e HOMA-IR (p < 0,05). A CC foi superior nos meninos dos dois grupos (p < 0,05) e só no Grupo PA alterada foram observados valores de HOMA-IR superiores entre meninas (p < 0,05). A correlação entre IMC e HOMA-IR no Grupo PA alterada foi moderada e significativa (ρ = 0,394; p < 0,001) e superior ao encontrado no Grupo PA normal. A correlação entre CC e HOMA-IR também foi significativa, moderada e semelhante em ambos os grupos (ρ = 0,345; p = < 0,05). Pela regressão logística, HOMA-IR foi preditor de alteração da PA (odds ratio - OR = 2,0; p = 0,001).

Conclusões:

Houve associação significativa entre resistência à insulina e PA com impacto desde a infância. A correlação e a associação entre os marcadores de risco cardiovasculares mais forte no Grupo PA alterada sugere que medidas de prevenção primária desses fatores de risco devem ser implementadas precocemente.

Palavras-chave:
Pressão Arterial; Índice de Massa Corporal; Resistência à Insulina; Antropometria; Adolescente

Introduction

Hypertension is one of the main risk factors for cardiovascular diseases, which are the main cause of deaths in Brazil and in the world.^1-3 In the last decade, high blood pressure levels have been identified in children and adolescents.^1,4-6

Obesity is highlighted as one of the important risk factors for hypertension, and it reaches epidemic proportions in many parts of the world.^7-9 Body fat mass is associated with profound changes in physiological functions, including from alterations in blood volume homeostasis to changes in left ventricular function. It is also indicated as a potential causal link between hypertension and insulin resistance (IR), among other metabolic changes.^8,10 It is estimated that 20%-30% of overweight / obese children and adolescents have hypertension.^11,12

Body composition is one of the main determinants of high blood pressure in childhood and adolescence. There is a direct relationship between weight, body mass index (BMI) and hypertension, particularly in the second decade of life.¹³

The strong association between high blood pressure and excessive weight has led to an increase in the prevalence of hypertension among children and adolescents.⁸ Waist circumference (WC) has a good predictive value for abdominal obesity-related diseases in adolescents, and increased WC values have been considered as a significant risk factor for IR and cardiovascular diseases.¹⁴

IR is also considered a risk marker for cardiovascular disease, and is associated with several metabolic changes related to, but not exclusively associated with obesity or type 2 diabetes.^15,16 For decades, abdominal fat has been associated with hyperinsulinemia, which is a predictor of hypertension and dyslipidemias.^9,17

The homeostasis model assessment as an index of IR (HOMA-IR) is a rapid, easy, low-cost method, which has been used as an alternative approach for IR diagnosis.¹⁹

There are no studies in Brazil correlating IR and blood pressure in adolescents aged over 12 years, and few studies have evaluated the correlation between IR and anthropometric variables in this population. The aim of this study was to evaluate the correlation between IR, WC, BMI and blood pressure in adolescents, and the behavior of these variables by sex.

Methods

This was a cross-sectional study, part of the original project CorAdo (Coração de Adolescente, Adolescent's heart). The study was approved by the local Ethics Committee (protocol: 017/2010), and conducted in a capital city of Brazil in 2012. The sample was representative of adolescent students, enrolled in the city's (public or private) schools.

In the initial sample of 1,025 adolescents, stratified by sex, anthropometric measurements were performed, as well as casual blood pressure and home blood pressure monitoring (HBPM).

WC was measured using a non-elastic measurement tape (200 cm). The cut-off points were adjusted by sex and age, and the 90th percentile was set as indicator of metabolic changes.²⁰

Body weight was measured to the nearest 0.1 kg using an electronic, portable scale (Kratos^®, 150 kg capacity), calibrated by the National Institute of Metrology, Quality and Technology (Inmetro). Height was measured to the nearest 0.1 cm using a wall-mounted stadiometer (Secca^®). All measurements were performed following the World Health Organization guidelines (WHO). ²¹

BMI was calculated by dividing body weight (kilograms) by the square of the height (meters).²² The adolescents were classified into obese or overweight based on WHO BMI cut-off points for age and sex (WHO).²³

Casual blood pressure and HBPM were measured using Omron HEM-705CP semi-automatic blood pressure monitors and different sizes of cuffs, in accordance to the 4^th Task Force's recommendations.²⁴

Four measures of casual blood pressure were taken, the first two measures when the blood pressure monitor was handed to patients, and the other two when patients returned the monitors one week later. There was a 3-min interval between measurements. The mean of the second readings was used for analysis. Blood pressure percentile was calculated using the formulas proposed by the 4^th Task Force, using the MeDCal 3000 software.

Adolescents and caregivers were instructed in the use of HBPM, to take four blood pressure measures, two in the morning (between 7h and 9h) and two in the afternoon (between 18h and 19h), with a 3-5 min-interval between them. One week later, participants returned the monitors, totaling 6 days of measurements.

The diagnosis of altered blood pressure (casual or HBPM) was determined according to international guidelines. Normal blood pressure was defined as having systolic pressure below the 90th percentile and blood pressure readings below 120/80 mmHg, and altered blood pressure was defined as systolic pressure greater than the 90th percentile.

Since there are no validated criteria for HBPM, we used the criteria proposed by the 4^th Task Force in the study by Stergiou et al.,²⁵ which suggests that both casual and HBPM measures should be similar in adolescents aged greater than 12 years.

Of the initial sample (n = 1,025), 198 (19.3%) adolescents had altered systolic and/or diastolic blood pressure in the casual measurement and/or HBPM, and composed the potential group for phase 2.

For sample size calculation, an error of 5% and power of 80% were fixed, considering the number of subjects with altered blood pressure (n= 198) identified from the initial sample during phase 1 of the CorAdo study. A minimum of 127 adolescents were required, and we also included 35 adolescents with normal blood pressure (controls), who were invited to the phase 2 of the study. A total of 162 adolescents completed the study (Figure 1).

Figure 1
Fluxogram of sample composition for the phase 2 of the study.

Participants' parents or caregivers signed the informed consent form before participating in the phase 2 of the study. Adolescents who met the inclusion criteria answered a questionnaire and had their blood collected.

Sexual maturation was assessed by self-assessment, using Tanner's photographs of five sexual maturation stages.²⁶ Children classified as prepubertal (Tanner stage I) were withdrawn from the study.

Inclusion criteria were adolescents aged from 12 to 18 years (to be completed), enrolled in public and private schools, with altered blood pressure (by casual measurement and/or HBPM), and Tanner stage ≥ 2 (pubertal stage).

Exclusion criteria included patients with physical disabilities that hinder blood pressure measurement, self-reported chronic disease, diabetes mellitus, kidney disease or heart disease, pregnancy, and chronic use of medications that may affect blood pressure, such as antihypertensive drugs, corticosteroids, antidepressants, anxiolytics, anti-inflammatories, and oral contraceptives.

Serum glucose and plasma insulin levels were determined. The HOMA-IR index (insulin µu/mL x glycemia mmol/L/22.5) was used to quantify IR, whose threshold set for adolescents is ≥ 3.16;²⁷ values of glycemia (mg/dL) were multiplied by 0.05551.^28,29

Statistical analysis

Statistical analysis was performed using the Statistical Package for Social Science (SPSS) software version 20 (IBM, Chicago, IL, USA) and Epi-Info^™. The Kolmogorov-Smirnov test was used to test the normality of the continuous variables and the Mann-Whitney U test to compare the means of the variables. Values were expressed as mean, median, standard deviation and confidence interval. A descriptive analysis of data was performed; associations between categorical variables were tested by the chi-square test, and the Spearman correlation was used to assess the association between blood pressure and BMI, WC, and HOMA-IR.

Stepwise regression was conducted, considering changes in blood pressure as dependent variable. In the bivariate analysis, variables with a p-value < 0.20 were considered predictors. The level of significance was set at p< 0.05.

Results

A total of 162 adolescents participated in the phase 2 of the study, 127 with altered blood pressure and 35 controls. Mean age of participants was 14.9 ± 1.62 years, and 61.1% were male.

Thirty-eight adolescents (23.5%) had altered HOMA-IR, 74 (45.7%) were overweight/obese, and 17 (10.5%) had increased WC (Table 1).

Table 1
Anthropometric and biochemical characteristics of the study group (n = 162)

Variables	n (%)	p value*
Waist circumference		0.005
Normal	145 (89.5)
Increased	17 (10.5)
Body mass index		< 0.001
Normal	88 (54.3)
Overweight	39 (24.1)
Obese	35 (21.6)
HOMA-IR		< 0.001
Normal	124 (76.5)
Altered	38 (23.5)

• ^*
  Chi-square test. HOMA-IR: Homeostasis Model Assessment - Insulin Resistance.

Mean values of HOMA-IR, BMI and WC were significantly higher in the group with altered blood pressure than in controls (Table 2).

Table 2
Blood pressure, Homeostasis Model Assessment - Insulin Resistance (HOMA-IR) index, waist circumference (WC) and body mass index (BMI) (n = 162)

Variables	Blood pressure				p value*
	Normal (n = 35)		Altered (n = 127)
	Mean	SD	Mean	SD
HOMA-IR	1.8	± 1.1	2.8	± 1.7	≤ 0.001
WC, cm	71.0	± 10.0	76.5	± 11.0	0.001
BMI, kg/m2	21.1	± 3.7	23.8	.8 ±	0.001

• ^*
  Mann-Whitney U test. SD: standard deviation.

When variables were categorized considering the normality criteria, a significant association was found only between blood pressure and BMI (p < 0.022), with 50.4% of participants with altered blood pressure and excessive weight, and no difference in sex distribution.

HOMA-IR index and BMI were similar between sexes. Mean WC was higher among male adolescents in both groups (altered blood pressure and normotensive) (p<0.05) (Tables 3 and 4). In the group of adolescents with altered blood pressure group, HOMA-IR indexes were higher in female than in male adolescents (p<0.05) (Table 4).

Table 3
Relationship between Homeostasis Model Assessment - Insulin Resistance (HOMA-IR), waist circumference (WC) and body mass index (BMI) in normotensive adolescents (n = 35)

Variables	Sex				p value*
	Male (n = 99)		Female (n = 63)
	Mean Mean	SD 95 % CI	Mean Median	SD 95 %CI
HOMA-IR	1.9	1.3	1.7	0.7	0.960
	1.5	0.65-6.12	1.5	0.7-3.4
WC, cm	74.2	11.2	65.8	4.4	0.009
	70.6	61-107	65.3	58.5-75.0
BMI, kg/m2	21.5	4.0	20.4	3.1	0.511
	20.6	17.0-30.7	19.6	16.8-26.3

• ^*
  Mann-Whitney U test. SD: standard deviation; 95%CI: 95% confidence interval.

Table 4
Relationship between Homeostasis Model Assessment - Insulin Resistance (HOMA-IR), waist circumference (WC) and body mass index (BMI) in adolescents with altered blood pressure (n = 127)

Variables	Sex				p value*
	Male (n = 99)		Female (n = 63)
	Mean Median	SD 95 %CI	Mean Median	SD 95 %CI
HOMA-IR	2.7	1.7	3.1	1.7	0.036
	2.2	0.53-8.39	2.7	0.61-8.57
WC, cm	78.1	10.9	74.1	10.7	0.035
	76.2	61-120	70.7	56-107
BMI, kg/m2	23.8	4.1	23.7	5.7	0.248
	23.4	15.9-35.0	22.5	16.1-42.5

• ^*
  Mann-Whitney U test. SD: standard deviation; 95%CI: 95% confidence interval.

There was a direct, moderate correlation between blood pressure and HOMA-IR (ρ = 0.323; p < 0.001), and a statistically significant but weak correlation between blood pressure and BMI, and between blood pressure and WC (ρ = 0.254; p = 0.001; e ρ = 0.258; p = 0.001).

In the group analysis, stronger correlations between variables were detected, especially between BMI and HOMA-IR in the group of altered blood pressure (ρ = 0.394; p < 0.001). Similar correlations between WC and HOMA-IR were found in both groups (ρ = 0.345; p < 0.05) (Table 5).

Table 5
Correlation of Homeostasis Model Assessment - Insulin Resistance (HOMA-IR) index, with body mass index (BMI) and waist circumference (WC) in adolescents with normotensive adolescents (n = 35) and altered blood pressure (n=127)

Variables	Normal blood pressure (n = 35)		Altered blood pressure (n = 127)
	Spearman	p value*	Spearman	p value*
HOMA-IR and BMI	0.366	0.031	0.394	< 0.001
HOMA-IR and WC	0.345	0.042	0.345	< 0.001

• ^*
  Spearman correlation test.

In the logistic regression analysis, blood pressure was affected only by HOMA-IR (odds ratio - OR = 2.0; p = 0.001).

Discussion

In many parts of the world, the prevalence of adult diseases, considered risk factors for cardiovascular diseases, has increased in pediatric population. Few studies have investigated the correlation/association between IR and blood pressure, especially in this population.

In this study, there was a positive association between mean values of HOMA-IR index and altered blood pressure in adolescents (p < 0.001). In the Bogalusa Heart Study, also conducted on adolescents, the HOMA-IR values were higher than those observed in our study. In another study carried out in Rio de Janeiro, the authors also reported higher HOMA-IR indexes, although the study group was composed of adults rather than adolescents.^30,31 In a pilot study conducted in Eastern Europe involving 128 children, HOMA-IR indexes were similar to our findings.³²

The prevalence of IR in our study group was 23.5%, considering a HOMA-IR cut-off point of 3.16, proposed by Keskin et al.²⁷ In Cochabamba, Bolivia, a study on 61 children and adolescents adopted³³ a different HOMA-IR cut-off (3.5), and reported a 39.4% prevalence of IR. A higher prevalence of IR was found in children and adolescents with high systolic pressure (p < 0.05).

In this study, HOMA-IR was not correlated with changes in blood pressure by using the absolute cut-off points. However, a significant direct correlation was found between mean HOMA-IR values and changes in blood pressure percentiles (ρ = 0.323; p < 0.001). This is in accordance with a study carried out in India, involving 2,640 adolescents.³⁴

Female adolescents with altered blood pressure had higher mean HOMA-IR values (p<0.05), which was not observed in the normotensive group. Previous studies^7,34 have reported a high prevalence of altered HOMA-IR among female adolescents, which may be in part explained by differences in body fat distribution or pubertal stages as compared with boys. With respect to sexual maturation, girls may enter puberty two years earlier than boys. In the absence of other known variables, these findings suggest that girls tend to be more resistance to insulin than boys due to sex-linked genes.³⁵

It is worth mentioning that previous studies have not reported differences in the mean values of HOMA-IR between sexes,^33,36 and one study has found a higher IR among boys than girls¹⁷. Further studies are needed to elucidate these conflicting results.

By logistic regression, our study identified, for the first time, that adolescents with altered HOMA-IR are twice as likely to have altered blood pressure (OR = 2.0; p = 0.001)

Other variables, such as BMI and WC did not affect the chance of having altered blood pressure. This result differed from that found in a study carried out in the south of Brazil on 1,950 children and adolescents, describing a positive relationship of systolic pressure to BMI and WC.^37,38

Some studies have reported an association between BMI and HOMA-IR, which may be explained by the increased anabolic effect of insulin and growth hormone related to the rapid somatic growth of children during puberty. This change in insulin sensitivity results from changes in body fat distribution in this period of life.^17,36

In the present study, a significant, moderate correlation was observed between BMI and HOMA-IR (ρ = 0.394; p < 0.001, for adolescents with altered blood pressure; and ρ = 0.366; p < 0.031, for normotensive adolescents. This is in accordance with previous investigations that showed that the prevalence of IR is more than twice as high among overweight and obese children and adolescents.^36,39,40

When analyzed by sex, we observed that male adolescents of both groups had higher mean WC, similarly to previous studies.^7,36

In addition, we found a positive correlation between WC and HOMA-IR (ρ = 0.345; p < 0.001 for altered blood pressure group; and ρ = 0.345; p = 0.042 for normotensive group). Singh and colleagues also found a strong correlation between HOMA-IR and WC,³⁶ and studies conducted in Brazil reported a significant association between WC and HOMA-IR in female adolescents.^39,41

Our study differs from previous studies in the analysis of correlations between variables (particularly HOMA-IR and BMI) by group, i.e. between adolescents with altered blood pressure and normotensive subjects.

The study has some limitations that need to be considered. First, the lack of a comprehensive assessment of body composition including other methods such as skinfold thickness or electrical bioimpedance analysis, and second, the possible inaccuracy of the method used for assessing sexual maturation.

Conclusion

There was a significant association of IR with blood pressure, and the impact of IR on blood pressure. The correlation and association between markers of cardiovascular diseases was more pronounced in adolescents with altered blood pressure, suggesting the need for primary prevention strategies for cardiovascular risk factors in childhood and adolescence.

• Sources of Funding
  This study was funded by CNpq.
• Study Association
  This article is part of the thesis of master submitted by Polyana Resende Silva de Morais, from Universidade Federal de Goiás.

Acknowledgements

We thank CNPq for the funding, and the Hypertension League of the Federal University of Goias (Liga de Hipertensão da Universidade Federal de Goiás), for all the support.

References

• ¹
  Koebnick C, Black MH, Wu J, Martinez MP, Smith N, Kuizon BD, et al. The prevalence of primary pediatric prehypertension and hypertension in a real-world managed care system. J Clin Hypertens (Greenwich). 2013;15(11):784-92.
• ²
  Ferrer M, Fernandez-Britto JE, Bacallao J, Perez H. Development of hypertension in a cohort of Cuban adolescents. MEDICC Rev. 2015;17(1):41-7.
• ³
  Campana EM, Brandão AA, Pozzan R, Magalhães ME, Fonseca FL, Pizzi OL, et al. Blood pressure in adolescence, adipokines and inflammation in young adults. The Rio de Janeiro study. Arq Bras Cardiol. 2014;102(1):60-9.
• ⁴
  Khoury M, Manlhiot C, McCrindle BW. Role of the waist/height ratio in the cardiometabolic risk assessment of children classified by body mass index. J Am Coll Cardiol. 2013;62(8):742-51.
• ⁵
  Corrêa Neto VG, Sperandei S, Silva LA, Maranhão Neto GA, Palma A. Arterial hypertension among adolescents in Rio de Janeiro: prevalence and association with physical activity and obesity. Ciênc Saúde Coletiva 2014;19(6):1699-708.
• ⁶
  Lo JC, Sinaiko A, Chandra M, Daley MF, Greenspan LC, Parker ED, et al. Prehypertension and hypertension in community-based pediatric practice. Pediatrics. 2013;131(2):e415-24.
• ⁷
  Juárez-Lopes C, Klunder-Klunder M, Medina-Bravo P, Madrigal-Azcárete A, Mass-Díaz E, Flores-Huerta S. Insulin resistance and its association with the components of the metabolic syndrome among obese children and adolescents. BMC Public Health. 2010;10:318.
• ⁸
  Kelishadi R, Poursafa P, Keramatian K. Overweight, air and noise pollution: Universal risk factors for pediatric pre-hypertension. J Res Med Sci. 2011;16(9):1234-50.
• ⁹
  Rocco ER, Mory DB, Bergamin CS, Valente F, Miranda VL, Calegare BF, et al. Optimal cutoff points for body mass index, waist circumference and HOMA-IR to identify a cluster of cardiometabolic abnormalities in normal glucose-tolerant Brazilian children and adolescents. Arq Bras Endocrinol Metabol. 2011;55(8):638-45.
• ¹⁰
  Chorin E, Hassidim A, Hartal M, Havakuk O, Flint N, Ziv-Baran T, et al. Trends in adolescents obesity and the association between BMI and blood pressure: a cross-sectional study in 714,922 healthy teenagers. Am J Hypertens. 2015;28(9):1157-63.
• ¹¹
  McNiece KL, Poffenbarger TS, Turner JL, Franco KD, Sorof JM, Portman RJ. Prevalence of hypertension and pre-hypertension among adolescents. J Pediatr. 2007;150(6):640-4, 644.e1.
• ¹²
  Jagadesan S, Harish R, Miranda P, Unnikrishnan R, Anjana RM, Mohan V. Prevalence of overweight and obesity among school children and adolescents in Chennai. Indian Pediatr. 2014;51(7):544-9.
• ¹³
  Andrade H, Antonio N, Rodrigues D, Da Silva M, Pêgo M, Providência LA. High blood pressure in the pediatric age group. Rev Port Cardiol. 2010;29(3):413-32.
• ¹⁴
  Costa JV, Silva AR, Moura IH, Carvalho RB, Bernardes LE, Almeida PC. An analysis of risk factors for arterial hypertension in adolescent students. Rev Lat Am Enfermagem. 2012;20(2):289-95.
• ¹⁵
  Kidambia S, Kotchena JM, Krishnaswamia S, Grima CE, Kotchena TA. Cardiovascular correlates of insulin resistance in normotensive and hypertensive African Americans. Metabolism. 2011;60(6):835-42.
• ¹⁶
  Raj M. Obesity and cardiovascular risk in children and adolescents. Indian J Endocrinol Metab. 2012;16(1):13-9.
• ¹⁷
  Kurtoglu S, Hatipoglu N, Mazicioglu M, Kendirici M, Keskin M, Kondolot M. Insulin resistance in obese children and adolescents: HOMA-IR cut-off levels in the prepubertal and pubertal periods. J Clin Res Pediatr Endocrinol. 2010;2(3):100-6.
• ¹⁸
  Vasques AC, Rosado L, Rosado G, Ribeiro Rde C, Francechini S, Geloneze B. Anthropometric indicators of insulin resistance. Arq Bras Cardiol. 2010;95(1):e14-23.
• ¹⁹
  Faria ER, Faria FR, Franceschini Sdo C, Peluzio Mdo C, Sant Ana LF, Novaes JF, et al. [Insulin resistance and components of metabolic syndrome, analysis by gender and stage of adolescence]. Arq Bras Endocrinol Metabol. 2014;58(6):610-8.
• ²⁰
  Freedman DS, Serdula MK, Srinivasan SR, Berenson GS. Relation of circumferences and skinfold thicknesses to lipid and insulin concentrations in children and adolescents: the Bogalusa Heart Study. Am J Clin Nutr. 1999;69(2):308-17.
• ²¹
  Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser. 1995;854:1-452.
• ²²
  Quetelet A. Anthropométrie ou mesure des différentes facultés de l'homme: Bruxelles: C. Muquardt; 1870.
• ²³
  de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85(9):660-7.
• ²⁴
  National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics. 2004;114(2 Suppl 4th Report):555-76.
• ²⁵
  Stergiou GS, Rarra VC, Yiannes NG. Changing relationship between home and office blood pressure with increasing age in children: the Arsakeion School study. Am J Hypertens. 2008;21(1):41-6.
• ²⁶
  Tanner JN. Growth at adolescence with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity. 2^nd ed. Oxford: Blackwell Scientific Publications; 1962.
• ²⁷
  Keskin M, Kurtoglu S, Kendirci M, Atabek ME, Yazici C. Homeostasis model assessment is more reliable than the fasting glucose/insulin ratio and quantitative insulin sensitivity check index for assessing insulin resistance among obese children and adolescents. Pediatrics. 2005;115(4):e500-3.
• ²⁸
  American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2006;29 Suppl 1:S43-8.
• ²⁹
  Wallace TM, Matthews DR. The assessment of insulin resistance in man. Diabet Med. 2002;19(7):527-34.
• ³⁰
  Srinivasan SR, Myers L, Berenson GS. Changes in metabolic syndrome variables since childhood in prehypertensive and hypertensive subjects: the Bogalusa Heart Study. Hypertension. 2006;48(1):33-9.
• ³¹
  Campana EM, Brandao AA, Pozzan R, Franca Mde F, Fonseca FL, Pizzi OL, et al. Blood pressure in young individuals as a cardiovascular risk marker. The Rio de Janeiro study. Arq Bras Cardiol. 2009;93(6):608-15, 657-65.
• ³²
  Pastucha D, Talafa V, Malincikova J, Cihalik C, Hyjanek J, Horakova D, et al. Obesity, hypertension and insulin resistance in childhood--a pilot study. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2010;154(1):77-81.
• ³³
  Caceres M, Teran CG, Rodriguez S, Medina M. Prevalence of insulin resistance and its association with metabolic syndrome criteria among Bolivian children and adolescents with obesity. BMC Pediatr. 2008;8:31.
• ³⁴
  Ramachandran A, Snehalatha C, Yamuna A, Murugesan N, Narayan KM. Insulin resistance and clustering of cardiometabolic risk factors in urban teenagers in southern India. Diabetes Care. 2007;30(7):1828-33.
• ³⁵
  Murphy MJ, Metcalf BS, Voss LD, Jeffery AN, Kirkby J, Mallam KM, et al; Early Bird Study (EarlyBird 6). Girls at five are intrinsically more insulin resistant than boys: The Programming Hypotheses Revisited--The EarlyBird Study (EarlyBird 6). Pediatrics. 2004;113(1 Pt 1):82-6.
• ³⁶
  Singh Y, Garg MK, Tandon N, Marwaha RK. A study of insulin resistance by HOMA-IR and its cut-off value to identify metabolic syndrome in urban Indian adolescents. J Clin Res Pediatr Endocrinol. 2013;5(4):245-51.
• ³⁷
  Burgos MS, Burgos LT, Camargo MD, Franke SI, Prá D, Silva AM, et al. Relationship between anthropometric measures and cardiovascular risk factors in children and adolescents. Arq Bras Cardiol. 2013;101(4):288-96.
• ³⁸
  Strufaldi MW, Silva EM, Puccini RF. Metabolic syndrome among prepubertal Brazilian schoolchildren. Diab Vasc Dis Res. 2008;5(4):291-7.
• ³⁹
  de Faria ER, Gontijo CA, Franceschini Sdo C, Peluzio Mdo C, Priore SE. Body composition and risk for metabolic alterations in female adolescents. Rev Paul Pediatr. 2014;32(2):207-15.
• ⁴⁰
  Velasco-Martinez RM, Jimenez-Cruz A, Higuera Dominguez F, Dominguez de la Piedra E, Bacardi-Gascon M. [Obesity and insulin resistance among adolescents from Chiapas]. Nutr Hosp. 2009;24(2):187-92.
• ⁴¹
  Pereira PF, Serrano HM, Carvalho GQ, Lamounier JA, Peluzio Mdo C, Franceschini Sdo C, et al. Waist and waist-to-height ratio: useful to identify the metabolic risk of female adolescents? Rev Paul Pediatr. 2011;29(3):372-7.

Publication Dates

• Publication in this collection
  22 Mar 2016
• Date of issue
  Apr 2016

History

• Received
  17 Aug 2015
• Reviewed
  11 Nov 2015
• Accepted
  19 Nov 2015