Revista Adolescência e Saúde

Revista Oficial do Núcleo de Estudos da Saúde do Adolescente / UERJ

NESA Publicação oficial
ISSN: 2177-5281 (Online)

Vol. 14 nº 3 - Jul/Sep - 2017

Original Article Imprimir 

Páginas 71 a 76

Assessment of Insulin Resistance in Adolescents with Different Nutritional Status

Evaluación de la Resistencia Insulínica en Adolescentes con Diferentes Estados Nutricionales

Avaliação da Resistência Insulínica em Adolescentes com Diferentes Estados Nutricionais

Autores: Soraya Nayra Sá Coêlho1; Nilviane Pires Silva Sousa2; Allan Kardec Barros3; Camila Guimarães Polisel4

1. Degree in Pharmacy (Pharmaceutical-Biochemical), Maranhão Federal University (UFMA). São Luís, Maranhão State, Brazil
2. Doctoral student in Biotechnology. Master`s Degree in Adult and Child Health, Maranhão Federal University (UFMA). São Luís, Maranhão State, Brazil
3. Post-Doctoral student, Institute of Physical and Chemical Engineering (RIKEN). Saitama, Japan. Professor, Electrical Engineering Department, Maranhão Federal University (UFMA). São Luís, Maranhão State, Brazil
4. PhD in Toxicology, Pharmaceutical Sciences College in Ribeirão Preto, São Paulo University (FCFRP-USP), Ribeirão Preto, São Paulo State, Brazil; and University of British Columbia (UBC), Vancouver, Canada.  Professor, Biological and Health Sciences Center, Mato Grosso do Sul Federal University (UFMS). Mato Grosso do Sul State, Brazil

Nilviane Pires Silva Sousa
Av. dos portugueses, 1966, Bacanga
São Luís, MA, Brasil. CEP: 65080-805

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Keywords: Adolescent, obesity, anthropometry, risk factors.
Palabra Clave: Adolescente, obesidad, antropometría, factores de riesgo.
Descritores: Adolescente, obesidade, antropometria, fatores de risco.

OBJECTIVE: Evaluate the prevalence of insulin resistance in adolescents with different nutritional status.
METHODS: This is a crosssectional study of 100 female adolescents with ages between 10 to 19 years regularly enrolled in public schools of São Luís/ MA. The variables evaluated were: weight, height, body mass index, fasting glucose and insulin. Insulin resistance was determined by the Homeostasis Model Assessment Insulin Resistance index. The study was approved by the Research Ethics Committee of the Universitary Hospital of the Federal University of Maranhão through the protocol number 251/11.
RESULTS: Participants were stratified into three groups according to nutritional status: obesity group - GOB (n = 25), overweight group - GSP (n = 38) and eutrophic group - GET (n =37). The prevalence of insulin resistance was 24.3% in the GET, 63.2% in GSP and 68% in the GOB.
CONCLUSION: A high prevalence of insulin resistance was observed in all nutritional status groups, which shows the importance of early diagnosis of the cardiometabolic risk factor and the need of health education for adolescents.

OBJETIVO: Evaluar la prevalencia de resistencia insulínica en escolares con diferentes estados nutricionales.
MÉTODOS: se trata de un estudio transversal realizado con 100 adolescentes del sexo femenino con edad entre 10 y 19 años, regularmente matriculadas en escuelas de la red pública de enseñanza de San Luís/MA. Las variables evaluadas fueron: peso, altura, índice de masa corporal, glicemia de ayuno e insulina. La resistencia a insulina fue determinada a través del índice Homeostasis Model Asesment sea Insulin Resistance. El estudio obtuvo la aprobación del Comité de Ética en Pesquisa del Hospital Universitario de la Universidad Federal de Maranhão, parecer 251/11.
RESULTADOS: Las participantes fueron estratificadas en tres grupos, de acuerdo con el estado nutricional: grupo obesidad - GOB (n=25), grupo sobrepeso - GSP (n=38) y grupo eutrófico - GET (n=37). La prevalencia de resistencia insulínica fue del 24,3% en el GET, 63,2% en el GSP y 68% en el GOB.
CONCLUSIÓN: Una alta prevalencia de resistencia insulínica fue identificada entre las adolescentes, lo que demuestra la importancia del diagnóstico precoz de ese factor de riesgo cardiometabólico, así como la necesidad de educación en salud en la adolescencia.

OBJETIVO: Avaliar a prevalência de resistência insulínica em escolares com diferentes estados nutricionais.
MÉTODOS: Tratase de um estudo transversal realizado com 100 adolescentes do sexo feminino com idade entre 10 e 19 anos regularmente matriculadas em escolas da rede pública de ensino de São Luís/MA. As variáveis avaliadas foram: peso, altura, índice de massa corporal, glicemia de jejum e insulina. A resistência à insulina foi determinada através do índice Homeostasis Model Assessment for Insulin Resistance. O estudo obteve a aprovação do Comitê de Ética em Pesquisa do Hospital Universitário da Universidade Federal do Maranhão, parecer 251/11.
RESULTADOS: As participantes foram estratificadas em três grupos, de acordo com o estado nutricional: grupo obesidade - GOB (n=25), grupo sobrepeso - GSP (n=38) e grupo eutrófico - GET (n=37). A prevalência de resistência insulínica foi de 24,3% no GET, 63,2% no GSP e 68% no GOB.
CONCLUSÃO: Uma alta prevalência de resistência insulínica foi identificada entre as adolescentes, o que demonstra a importância do diagnóstico precoce desse fator de risco cardiometabólico, bem como a necessidade de educação em saúde na adolescência.


Obesity during childhood and adolescence is a complex public health problem that has expanded during the past few decades all over the world1. The report on Ending Childhood Obesity2 indicated the number of overweight children in low to medium income countries more than doubled between 1990 and 2014, climbing from 7.5 to 15.5 million. Brazil´s Family Budget Survey3 (POF 2008-2009) indicated that obesity affects 5.8% of boys and 4.0% of girls between 10 and 19 years of age.

Obesity and metabolic disease rates are alarming all over the world, affecting steadily increasing numbers of children and adolescents1. Clinical and epidemiological studies have shown that body fat distribution is related to cardiovascular risk factors in adults, as well as children and adolescents1.

The Body Mass Index (BMI) is the most widely used tool for diagnosing obesity, with the World Health Organization (WHO) establishing BMI reference standards for age and gender, recommending its use to assess children and adolescents everywhere, regardless of ethnicity, social and economic status or type of diet4. The BMI has been widely used to identify adiposity in children and adolescents, as it is easy to obtain data at low cost, presenting a good correlation with body fat5.

Overweight may step up the risks of developing metabolic alterations such as dyslipidemias, insulin resistance (IR), reduced glucose tolerance and high blood pressure6. Insulin resistance is characterized by weak insulin action7 resulting from a reduction in its ability to stimulate glucose use. Pancreatic b-cells step up insulin production and secretion as a compensatory mechanism (hyperinsulinemia) while glucose tolerance remains normal8. Insulin resistance has been rated as a collective health problem that even affects children and adolescents8.

Evidence indicates that IR is common among children9 and adolescents and, as homeostatic model assessment (HOMA) is a reliable tool that is widely used to measure IR in adolescents9-11, this study intends to assess the presence of IR among schoolchildren in São Luís, Maranhão State, Northeast Brazil.



This cross-sectional research project was conducted between 2011 and 2013, with a sample of 100 adolescents calculated on the basis of an obesity rate of 4.0%among girls (POF 2008-2009), which is the proportion suggested by a 10.0% result, and acceptable error rate of 5% and an 80% test power10, with an additional 10% to cover losses or refusals. The sample was taken from the population of nine schools in the Federal, State and Municipal education network in São Luís, Maranhão State, selected at random, consisting of girls between 10 and 19 years of age. The following exclusion criteria were used: pregnancy, breastfeeding, taking contraceptives, pre-menarchal and physical disabilities preventing or adversely affecting anthropometric measurements.

The Ethics Committee for Research involving Human Beings at the Maranhão Federal University Hospital (HUUFMA) approved this study under Opinion Nº 251/11.


All the variables were measured by trained evaluators using calibrated equipment in a specially-prepared well-ventilated room to which the respondents were sent before class. The anthropometric measurements, including weight and height, were obtained through standardized techniques by trained researchers. All the measurements were taken twice, working with the mean figures for the data analysis. Weight was measured on an electronic scale (Seca® 803) in 0.1 kg increments.  Height was measured through a portable vertical stadiometer (Seca® 213), with 1 mm increments. BMI was calculated as weight divided by height squared (kg/m²).  Based on the percentile for gender and age established by the WHO11, the adolescents were divided into categories by nutritional status as follows: eutrophic ≥ percentile (p) 3 and < percentile (p) 85, overweight ≥ p 85 and < p 97 and obese ≥ p 97.

Blood was taken after fasting for twelve hours, with the samples analyzed in the Clinical Analysis Laboratory at the Maranhão Federal University Hospital, using Cobas 6000 equipment made by Roche®.  Insulinemia was assessed through the electrochemoluminescence method, with the adopted reference values12 being: normal < 15 µm/L, borderline 15 to 20 µm/L and high > 20 µm/L.  Fasting blood sugar was assessed through the enzymatic colorimetric method, with the benchmark value13 established at ≤ 100 mg/dL. The HOMA was calculated through the product of the following ratios: fasting blood sugar (mg/dL) divided by 18 and insulin (µU/mL) divided by 22.5.  The HOMA values 12 were rated as high when above 3.16, thus indicating the presence of IR.

Statistical Analysis

For the statistical analysis and data file, the Statistical Package for the Social Sciences (SPSS) software was used, version 19.0. The data were treated through descriptive procedures, calculating the mean and median figures, as well as the standard deviation. The normal data distribution was ascertained through the Kolmogorov-Smirnov test, with the ANOVA one-way variance analysis used for comparing the body mass and glycemia variables for different nutritional status, followed by the Bonferronni post hoc multiple comparison test in order to locate possible differences among the groups.  The Kruskal-Wallis test was used to compare the age, height, BMI, HOMA and insulin variables among the nutritional status groups. The significance level was established at 5%.


This study encompassed 100 girls with a mean age of 14.08±1.8 years old, stratified into three groups by nutritional status (BMI): eutrophic group - GET (n=37), overweight group - GSP (n=38) and obese group - GOB (n=25). Only the body mass and BMI anthropometrics variables presented statistically significant differences by group (Table 1). All the respondents in this study presented normal blood sugar levels, although a significant difference (p=0.001) was noted in the glycemic levels of the groups, indicating that higher fasting blood sugar levels were found among adolescents with higher BMI (Table 2). Furthermore, Table 2 also showed a steady and statistically significant increase in the mean values for the insulin variable as well as for the HOMA, from the GET to the GSP, and then to the GOB. Analyzing each of the groups in greater detail, a high proportion of hyperinsulemic adolescents was also noted at 26% (n=26) of the sample, being more prevalent among obese girls (Table 3). The prevalence of IR was higher in the obese group (Table 4).


Similar to this study, Serrano et al. (2010)14 analyzed 113 adolescent girls in government schools, finding higher fasting blood sugar levels in the obese group (82 mg/dL) compared to the normal weight group (76 mg/dL). Observing these results, this suggests that the control of metabolic alterations must begin during childhood and adolescence, as although hyperinsulinemia can outweigh IR, glycemia will remain within the benchmark values, unless other factors such as prolonged exposure to hyperinsulinemia may lead to depletion of the pancreatic beta cells, consequently leading to the appearance of insulin resistance, glucose intolerance and Type 2 diabetes15, 16.

For hyperinsulinemia, similar results were found by Serrano et al. (2010)14 who observed: hyperinsulinemia in 15.8% and IR in 15.7% of eutrophic adolescents with excess body fat, hyperinsulinemia in 7.5% and IR in 2.5% of eutrophic adolescents with body fat within normal levels and 45.7% for hyperinsulinemia and IR among overweight adolescents with excess body fat.

Pinho et al. (2012)17 assessed 69 girls with differing nutritional status, also observing that hyperinsulinemia was present among adolescents at normal weights, but riding in parallel to the BMI. Generally defined by the BMI, overweight is associated with metabolic disorders (such as glucose intolerance, type 2 diabetes mellitus and dyslipidemia).

However, more than the total quantity of adipose tissue, its distribution in the body is also a risk indicator for developing these diseases7. A build-up of fat in the abdominal region and in non-adipose tissue (ectopic fat) for example, is associated with a higher risk of metabolic disorders. On the other hand, observations suggest that people with peripheral adiposity, characterized by increased hip and thigh circumferences, have better glucose tolerance, lower levels of type 2 diabetes and less metabolic syndrome7.  One of the alterations underlying the link between obesity, particularly in the visceral, and the disorders listed above is insulin resistance7.

The reason why IR is worsened by obesity is due to the fact that white fat tissue serves as a complex endocrine organ that secretes substances (adipokines) through adipocytes, thus participating in various metabolic activities such as appetite regulation and glucose metabolism, among others18. The adipokines may trigger inflammatory actions that influence the intracell insulin pathway, with adverse effects on the translocation of GLUT 4 to the plasma membrane19, reducing the capacity of skeletal muscle and other tissues able to take up glucose for the cells, leading to a hyperglycemic status19. These insulin-signaling alterations are essential for the development of metabolic syndrome. These disorders may play a role in the appearance of cardiovascular disease in metabolic syndrome and the development of vascular complications of diabetes, creating a context of hyperglycemia, dyslipidemia, high blood pressure and inflammation. However, abnormal insulin signs in arteries, vascular cells and others in the heart, kidney and retina also contribute to the disease in these tissues20.


This study identified the presence of metabolic alterations in all the nutritional status groups, including the eutrophic adolescent group. The presence of hyperinsulinemia and IR in all these groups underscores the importance of early diagnosis for cardiovascular risk factors and health education actions intended mainly to encourage changes in adolescent lifestyles, especially those related to the development of healthier eating habits, physical exercise and bodyweight control, in order to avoid the appearance of obesity and associated comorbidities during adulthood.


The authors thank the school administrators, the pupils and their respective parents and guardians for their contributions to this study.


1. Sousa NPS, Salvador EP, Barros AK, Polisel CG, Carvalho WRG. Anthropometric Predictors of Abdominal Adiposity in Adolescents. JEPonline 2016;19(4):66-76.

2. Organização Mundial da Saúde. Ending Childhood Obesity (ECHO). Geneva: OMS, 2016.

3. Instituto Brasileiro de Geografia e Estatística - IBGE. Antropometria e estado nutricional de crianças e adolescentes e adultos no Brasil. Pesquisa de Orçamento Familiar. Ministério da Saúde, 2010.

4. Rerksuppaphol S, Rerksuppaphol L. Waist Circunference, Waist-to-Height Ratio and Body Mass Index of Thai Children: Secular Cahnges and Updated Reference Satandards. Journal of Clinical and Diagnostic Research 2014; 8(11), PC05-PC09.

5. Oliveira JR, Frutuoso MFP, Gambardella AMD. Association among sexual maturation, overweight and central adiposity in children and adolescents at two schools in São Paulo. Rev. Bras. Crescimento Desenvolv. Hum 2014; 24 (2): 201-207.

6. Faria ER, Contijo CA, Franceschini SCC, Peluzio MCG, Priore SE. Composição corporal e risco de alterações metabólicas em adolescentes do sexo feminino. Rev Paul Pediatr 2014; 32 (2); 207-215.

7. Castro AVB, Kolka CM, Kim SP, Bergman RN. Obesity, insulin resistance and comorbidities? Mechanisms of association. Arq Bras Endocrinol Metab 2014; 58 (6): 600-609.

8. Gobato AO, Vasques ACJ, Zambon MP, Filho AAB, Hessel G. Metabolic Syndrome and insulin resistence in obese adolescents. Rev Paul Pediatr 2014; 32 (1): 55-62.

9. Wang L, Wang H, Wen H, Tao H, Zhao X. Relationship between HOMA-IR and serum vitamin D in Chinese children and adolescents. J Pediatr Endocrinol Metab 2016; 1-5. DOI: 10.1515/jpem-2015-0422.

10. Lwanga SK, Lemeshow S. Sample size determination in health studies: a practical manual. World Health Organization, 1991.

11. WHO. Organização Mundial da Saúde. Child Growth Standards: length/height-for-age, weight-for age, weight-for-length, weight-for-height and body mass index-for-age. Methods and development. WHO (nonserial publication). Geneva: WHO; 2006/2007.

12. Sociedade Brasileira de Cardiologia. I Diretriz de prevenção de arterosclerose na infância e na adolescência. ArqBrasCardiol 2005; 85(Supl. VI).

13. Sociedade Brasileira de Diabetes. Diretrizes da sociedade brasileira de diabetes: 2013-2014. São Paulo: AC farmacêutica 2014; 22-23.

14. Serrano HMS, Carvalho GQ, Pereira PF, Peluzio MCG, Franceschini, SCC, Priore SE. Composição corpórea, alterações bioquímicas e clínicas de adolescentes com excesso de adiposidade. ArqBrasCardiol 2010; 95(4):464-472.

15. Robins, KumarVinay, Abbas Jon C. Patologia básica. 2008. Editora Elsevier, 8ª edição, cap.20, 2008.

16. Venturini CD, Engroff P, Gomes I, Carli GA. Prevalência de obesidade associada à ingestão calórica, glicemia e perfil lipídico em uma amostra populacional de idosos do Sul do Brasil. Rev Bras Geriatr Gerontol 2013;16 (3): 591-601.

17. Pinho AP, Brunetti IL, Pepato MT, Almeida CAN. Síndrome metabólica em adolescentes do sexo feminino com sobrepeso e obesidade. Rev Paul Pediat 2012; 30(1): 51-56.

18. Sawaya AL, Lenadro CVG, Waitzberg D. Fisiologia da Nutrição e na Doença: da Biologia Molecular ao Tratamento. São Paulo: Ed. Atheneu, 2013.

19. Freitas MC, Ceschini FL, Ramallo BT. Insulin resistance associated with obesity: anti-inflammatory effects of physical exercise. R Bras Ci e Mov 2014; 22(3): 139-174.

20. Rask-Madsen C., Ronald Kahn C. Tissue-specific insulin signaling, metabolic syndrome and cardiovascular disease. Arterioscler ThrombVasc Biol 2012; 32(9): 2052-2059. DOI:10.1161/ATVBAHA. 111.241919.
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