Skip to main content
Top
Published in: BMC Cardiovascular Disorders 1/2018

Open Access 01-12-2018 | Research article

Metabolically healthy and metabolically unhealthy obese children both have increased carotid intima-media thickness: a case control study

Authors: Giovanni Farello, Annarita Antenucci, Stefano Stagi, Chiara Mazzocchetti, Franco Ciocca, Alberto Verrotti

Published in: BMC Cardiovascular Disorders | Issue 1/2018

Login to get access

Abstract

Background

The cardiovascular disease risk was assessed in metabolically healthy obese (MHO) children, obese children with metabolic disorders (MUO), and to a control group of normal-weight children using carotid intima-media thickness (CIMT).

Methods

Participants were 204 obese children (114 M, 90 F), including 162 MUO (74 M, 88 F) and 42 MHO (24 M, 18 F), and 99 gender- and age-matched controls (45 M, 54 F). Glucose, triglycerides, total cholesterol, high-density and low-density lipoprotein cholesterol, and other serum values were determined in peripheral blood. Anthropometric parameters, blood pressure, and a carotid Doppler ultrasound scan were also acquired. The mean CIMT of obese subjects and controls was compared by analysis of variance. Abnormality of even one of the metabolic parameters assessed involved assignation to the MUO group. Mean CIMT was compared in MHO and MUO children.

Results

Mean CIMT in control children was 402.97 ± 53.18 μm (left carotid artery) and 377.85 ± 52.47 μm (right carotid artery). In MHO and MUO patients CIMT was respectively 453.29 ± 62.04 and 460.17 ± 92.22 μm (left carotid artery) and 446.36 ± 49.21 and 456.30 ± 85.7 μm (right carotid artery). The mean CIMT was not significantly different in MUO and MHO children, whereas it showed a significant difference between both groups of obese children and controls (p < 0.01).

Conclusion

CIMT was significantly greater in obese patients, also in those without metabolic alterations, than in normal-weight children. Obesity is therefore an important risk factor for cardiovascular disease in itself, also in the absence of metabolic abnormalities.
Literature
1.
go back to reference WHO, Regional Office for Europe. Country profiles on nutrition. Phisical activity and obesity in the 53 WHO European Region Member States: Methodology and summary. 2013;1–9. WHO, Regional Office for Europe. Country profiles on nutrition. Phisical activity and obesity in the 53 WHO European Region Member States: Methodology and summary. 2013;1–9.
2.
go back to reference Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes. 1988;37:1595–607.CrossRefPubMed Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes. 1988;37:1595–607.CrossRefPubMed
4.
go back to reference Friend A, Craig L, Turber S. The prevalence of metabolic syndrome in children: a systematic review of the literature. Metab Syndr Relat Disord. 2013;11:71–80.CrossRefPubMed Friend A, Craig L, Turber S. The prevalence of metabolic syndrome in children: a systematic review of the literature. Metab Syndr Relat Disord. 2013;11:71–80.CrossRefPubMed
5.
go back to reference Sims EA. Are there person who are obese, but metabolically healthy? Metabolism. 2001;50(12):1499–504.CrossRefPubMed Sims EA. Are there person who are obese, but metabolically healthy? Metabolism. 2001;50(12):1499–504.CrossRefPubMed
6.
go back to reference Bluher M. The distinction of metabolically ‘healthy’ from ‘unhealthy’ obese individuals. Curr Opin Lipidol. 2010;21(1):38–43.CrossRefPubMed Bluher M. The distinction of metabolically ‘healthy’ from ‘unhealthy’ obese individuals. Curr Opin Lipidol. 2010;21(1):38–43.CrossRefPubMed
7.
go back to reference Bluher S, Schwarz P. Metabolically healthy obesity from childhood to adulthood - does weight status alone matter? Metabolism. 2014;63:1084–92.CrossRefPubMed Bluher S, Schwarz P. Metabolically healthy obesity from childhood to adulthood - does weight status alone matter? Metabolism. 2014;63:1084–92.CrossRefPubMed
8.
go back to reference Rey-Lopez JP, de Rezende LF, Pastor-Valero M, et al. The prevalence of metabolically hralthy obesity: a systematic review and critical evaluation of the definitions used. Obes Rev. 2014;15(10):781–90.CrossRefPubMed Rey-Lopez JP, de Rezende LF, Pastor-Valero M, et al. The prevalence of metabolically hralthy obesity: a systematic review and critical evaluation of the definitions used. Obes Rev. 2014;15(10):781–90.CrossRefPubMed
9.
go back to reference Camhi S, Waring M, Sisson S, et al. Physical activity and screen time in metabolically healthy obese phenotypes in adolescents and adults. J Obes. 2013;984613:1–9. Camhi S, Waring M, Sisson S, et al. Physical activity and screen time in metabolically healthy obese phenotypes in adolescents and adults. J Obes. 2013;984613:1–9.
10.
go back to reference Urbina EM, Williams RV, Alpert BS, Collins RT, Daniels SR, Hayman L, American Heart Association Atherosclerosis, Hypertension, and Obesity in Youth Committee of the Council on Cardiovascular Disease in the Young, et al. Noninvasive assessment of subclinical atherosclerosis in children and adolescents: recommendations for standard assessment of clinical research: a scientific statement from the American Heart Association. Hypertension. 2009;54(5):919–50.CrossRefPubMed Urbina EM, Williams RV, Alpert BS, Collins RT, Daniels SR, Hayman L, American Heart Association Atherosclerosis, Hypertension, and Obesity in Youth Committee of the Council on Cardiovascular Disease in the Young, et al. Noninvasive assessment of subclinical atherosclerosis in children and adolescents: recommendations for standard assessment of clinical research: a scientific statement from the American Heart Association. Hypertension. 2009;54(5):919–50.CrossRefPubMed
11.
go back to reference Chen W, Srinivasan SR, Li S, Xu J, Berenson GS. MetS variables at low levels in childhood are beneficially associated with adulthood cardiovascular risk: the Bogalusa heart study. Diab Care. 2005;28:126–31.CrossRef Chen W, Srinivasan SR, Li S, Xu J, Berenson GS. MetS variables at low levels in childhood are beneficially associated with adulthood cardiovascular risk: the Bogalusa heart study. Diab Care. 2005;28:126–31.CrossRef
12.
go back to reference Raitakari OT, Juonala M, Kahonen M, et al. Cardiovascular risk factors in childhood and carotid artery intima–media thickness in adulthood: the cardiovascular risk in young Finns study. JAMA. 2003;290:2277–83.CrossRefPubMed Raitakari OT, Juonala M, Kahonen M, et al. Cardiovascular risk factors in childhood and carotid artery intima–media thickness in adulthood: the cardiovascular risk in young Finns study. JAMA. 2003;290:2277–83.CrossRefPubMed
13.
go back to reference Lorenz MW, Markus HS, Bots ML, et al. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007;115(4):459–67.CrossRefPubMed Lorenz MW, Markus HS, Bots ML, et al. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007;115(4):459–67.CrossRefPubMed
14.
go back to reference Bland J, Skordalaki A, Emery JL. Early intimal lesions in the common carotid artery. Cardiovasc Res. 1986;20:863–8.CrossRefPubMed Bland J, Skordalaki A, Emery JL. Early intimal lesions in the common carotid artery. Cardiovasc Res. 1986;20:863–8.CrossRefPubMed
15.
go back to reference Mansia G, De Backer G, Dominiczak A, et al. European Society of Hypertension; European Society of Cardiology. 2007 ESH-ESC guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Blood Press. 2007;16(3):135–232.CrossRefPubMed Mansia G, De Backer G, Dominiczak A, et al. European Society of Hypertension; European Society of Cardiology. 2007 ESH-ESC guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Blood Press. 2007;16(3):135–232.CrossRefPubMed
16.
go back to reference Lamotte C, Iliescu C, Libersa C, et al. Increased intima-media thickness of the carotid artery in childhood: a systematic review of observational studies. Eur J Pediatr. 2011;170:719–29.CrossRefPubMed Lamotte C, Iliescu C, Libersa C, et al. Increased intima-media thickness of the carotid artery in childhood: a systematic review of observational studies. Eur J Pediatr. 2011;170:719–29.CrossRefPubMed
17.
go back to reference Reinehr T, Wunsch R, Pütter C, et al. Relationship between carotid intima-media thickness and metabolic syndrome in adolescents. J Pediatr. 2013;163(2):327–32.CrossRefPubMed Reinehr T, Wunsch R, Pütter C, et al. Relationship between carotid intima-media thickness and metabolic syndrome in adolescents. J Pediatr. 2013;163(2):327–32.CrossRefPubMed
18.
go back to reference Dalla Pozza R, Schetitska DE, Fritsch P, et al. Intima media thickness measurement in children: a statement from the Association for European Paediatric Cardiology (AEPC) working group on cardiovascular prevention endorsed by the Association for European paediatric cardiology. Atherosclerosis. 2015;238:380–7.CrossRefPubMed Dalla Pozza R, Schetitska DE, Fritsch P, et al. Intima media thickness measurement in children: a statement from the Association for European Paediatric Cardiology (AEPC) working group on cardiovascular prevention endorsed by the Association for European paediatric cardiology. Atherosclerosis. 2015;238:380–7.CrossRefPubMed
19.
go back to reference Li S, Chen W, Srinivasan S, et al. Relation if childhood obesity/cardiometabolic phenotypes to adult cardiometabolic profile: the Bogalusa heart study. Am J Epidemiol. 2012;176(7):S142–9.CrossRefPubMedPubMedCentral Li S, Chen W, Srinivasan S, et al. Relation if childhood obesity/cardiometabolic phenotypes to adult cardiometabolic profile: the Bogalusa heart study. Am J Epidemiol. 2012;176(7):S142–9.CrossRefPubMedPubMedCentral
20.
go back to reference Mangge H, Zelzer S, Puerstner P, et al. Uric acid best predicts metabolically unhealthy obesity with increased cardiovascular risk in youth and adults. Obesity. 2013;21(1):E71–7.CrossRefPubMed Mangge H, Zelzer S, Puerstner P, et al. Uric acid best predicts metabolically unhealthy obesity with increased cardiovascular risk in youth and adults. Obesity. 2013;21(1):E71–7.CrossRefPubMed
21.
go back to reference Koskinen J, Magnussen CG, Sabin MA, et al. Youth overweight and metabolic disturbances in predicting carotid intima-media thickness, type 2 diabetes, and metabolic syndrome in adulthood: the cardiovascular risk in young Finns study. Diabetes Care. 2014;37(7):1870–7.CrossRefPubMed Koskinen J, Magnussen CG, Sabin MA, et al. Youth overweight and metabolic disturbances in predicting carotid intima-media thickness, type 2 diabetes, and metabolic syndrome in adulthood: the cardiovascular risk in young Finns study. Diabetes Care. 2014;37(7):1870–7.CrossRefPubMed
22.
go back to reference Zimmet P, Alberti KG, Kaufman F, Tajima N, Silink M, Arslanian S, et al. The metabolic syndrome in children and adolescents - an IDF consensus report. Pediatr Diabetes. 2007;8:299–306.CrossRefPubMed Zimmet P, Alberti KG, Kaufman F, Tajima N, Silink M, Arslanian S, et al. The metabolic syndrome in children and adolescents - an IDF consensus report. Pediatr Diabetes. 2007;8:299–306.CrossRefPubMed
23.
go back to reference Khokhar A, Chin V, Perez-Colon S, Farook T, Bansal S, Kochummen UV. Differences between metabolically healthy vs unhealthy obese children and adolescents. J Natl Med Assoc. 2017;109:203–10.CrossRefPubMed Khokhar A, Chin V, Perez-Colon S, Farook T, Bansal S, Kochummen UV. Differences between metabolically healthy vs unhealthy obese children and adolescents. J Natl Med Assoc. 2017;109:203–10.CrossRefPubMed
24.
go back to reference Cacciari E, Milani S, Balsamo A, and SIEDP Directive Council 2002-03. Italian cross sectional growth charts for height, weight and BMI (2 to 20 yr). Endocrinol Invest. 2006;29:581–93.CrossRef Cacciari E, Milani S, Balsamo A, and SIEDP Directive Council 2002-03. Italian cross sectional growth charts for height, weight and BMI (2 to 20 yr). Endocrinol Invest. 2006;29:581–93.CrossRef
25.
go back to reference Report of a WHO Expert Consultation: Waist Circumference and Waist–Hip Ratio. Geneva, 8–11 December 2008. Report of a WHO Expert Consultation: Waist Circumference and Waist–Hip Ratio. Geneva, 8–11 December 2008.
26.
go back to reference Maffeis C, Banzato C, Talamini G. Waist-to-height ratio, a useful index to identify high metabolic risk in overweight children. J Pediatr. 2008;152:207–13.CrossRefPubMed Maffeis C, Banzato C, Talamini G. Waist-to-height ratio, a useful index to identify high metabolic risk in overweight children. J Pediatr. 2008;152:207–13.CrossRefPubMed
27.
go back to reference Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.CrossRefPubMed Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.CrossRefPubMed
28.
go back to reference Faul F, Erdfelder E, Lang A-G, Buchner A. G*power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.CrossRefPubMed Faul F, Erdfelder E, Lang A-G, Buchner A. G*power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.CrossRefPubMed
29.
go back to reference Chambless LE, Heiss G, Folsom AR, Rosamond W, Szklo M, Sharrett AR, et al. Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the atherosclerosis risk in communities (ARIC) study, 1987-1993. Am J Epidemiol. 1997;146:483–94.CrossRefPubMed Chambless LE, Heiss G, Folsom AR, Rosamond W, Szklo M, Sharrett AR, et al. Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the atherosclerosis risk in communities (ARIC) study, 1987-1993. Am J Epidemiol. 1997;146:483–94.CrossRefPubMed
30.
go back to reference Hodis HN, Mack WJ, La Bree L, Selzer RH, Liu CR, Liu CH, et al. The role of carotid arterial intima-media thickness in predicting clinical coronary events. Ann Intern Med. 1998;128:262–9.CrossRefPubMed Hodis HN, Mack WJ, La Bree L, Selzer RH, Liu CR, Liu CH, et al. The role of carotid arterial intima-media thickness in predicting clinical coronary events. Ann Intern Med. 1998;128:262–9.CrossRefPubMed
31.
go back to reference Polak JF, Pencina MJ, Pencina KM, O’Donnel CJ, Wolf PA, D’Agostino RB. Carotid intima-media thickness and cardiovascular events. N Engl J Med. 2011;365:213–21.CrossRefPubMedPubMedCentral Polak JF, Pencina MJ, Pencina KM, O’Donnel CJ, Wolf PA, D’Agostino RB. Carotid intima-media thickness and cardiovascular events. N Engl J Med. 2011;365:213–21.CrossRefPubMedPubMedCentral
32.
go back to reference Roberson LL, Aneni EC, Maziak W, Agatson A, Feldman T, Roussef M, Tran T, Blaha MJ, Santos RD, Sposito A, Al-Mallah MH, Blankstein R, Budoff JM, Nasir K. Beyond BMI: the “metabolic healthy obese” phenotype & its association with clinical/subclinical cardiovascular disease and all-cause mortality – a systematic review. BMC Public Health. 2014;14:14.CrossRefPubMedPubMedCentral Roberson LL, Aneni EC, Maziak W, Agatson A, Feldman T, Roussef M, Tran T, Blaha MJ, Santos RD, Sposito A, Al-Mallah MH, Blankstein R, Budoff JM, Nasir K. Beyond BMI: the “metabolic healthy obese” phenotype & its association with clinical/subclinical cardiovascular disease and all-cause mortality – a systematic review. BMC Public Health. 2014;14:14.CrossRefPubMedPubMedCentral
33.
go back to reference Zamrazilova H, Weiss R, Hainer V, Aldhoon-Hainerová I. Cardiometabolic health in obese adolescents is related to length of obesity exposure: a pilot study. J Clin Endocrinol Metab. 2016;101:3088–95.CrossRefPubMed Zamrazilova H, Weiss R, Hainer V, Aldhoon-Hainerová I. Cardiometabolic health in obese adolescents is related to length of obesity exposure: a pilot study. J Clin Endocrinol Metab. 2016;101:3088–95.CrossRefPubMed
34.
go back to reference Fernandez JR, Redden D, Pietrobelli A, et al. Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr. 2004;145:439–44.CrossRefPubMed Fernandez JR, Redden D, Pietrobelli A, et al. Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr. 2004;145:439–44.CrossRefPubMed
35.
go back to reference Shashaj B, Luciano R, Contoli B, et al. Reference ranges of HOMA-IR in normal-weight and obese young Caucasians. Acta Diabetol. 2016;53:251–60.CrossRefPubMed Shashaj B, Luciano R, Contoli B, et al. Reference ranges of HOMA-IR in normal-weight and obese young Caucasians. Acta Diabetol. 2016;53:251–60.CrossRefPubMed
36.
go back to reference Daniels SR, Greer FR. The committee on nutrition. Lipid screening and cardiovascular health in childhood. Pediatrics. 2008;122:198–208.CrossRefPubMed Daniels SR, Greer FR. The committee on nutrition. Lipid screening and cardiovascular health in childhood. Pediatrics. 2008;122:198–208.CrossRefPubMed
37.
go back to reference 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. 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.
Metadata
Title
Metabolically healthy and metabolically unhealthy obese children both have increased carotid intima-media thickness: a case control study
Authors
Giovanni Farello
Annarita Antenucci
Stefano Stagi
Chiara Mazzocchetti
Franco Ciocca
Alberto Verrotti
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Cardiovascular Disorders / Issue 1/2018
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-018-0874-5

Other articles of this Issue 1/2018

BMC Cardiovascular Disorders 1/2018 Go to the issue