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Archives of Medical Science
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vol. 14
Clinical research

Is subclinical atherosclerosis associated with visceral fat and fatty liver in adolescents with type 1 diabetes?

Hoda Atwa, Khaled Gad, Hala Hagrasy, Amany Elkelany, Mona Azzam, Nouran Bayoumi, Ayman Gobarah, Hassan Shora

Arch Med Sci 2018; 14, 6: 1355–1360
Online publish date: 2018/03/12
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There is a 3-fold higher prevalence of cardiovascular complications in patients with type 1 diabetes. The aim was to assess the relationship between subclinical atherosclerosis and visceral fat and fatty liver in diabetic adolescents.

Material and methods
The study was performed on 110 adolescents with type 1 diabetes (T1D) attending the Pediatric Diabetes Clinic of the University Hospital, Ismailia, Egypt. Their mean age was 14.2 ±0.7 years with a mean duration of diabetes 6 ±0.3 years. They were divided into group 1 which consisted of 55 adolescents with T1D and normal carotid intima media thickness (cIMT) and the second group which included 55 adolescents with T1D and subclinical atherosclerosis. All adolescents were normotensive, normo-albuminuric and had no retinopathy. Visceral fat thickness was measured as the distance between the anterior wall of the aorta and the posterior surface of the rectus abdominis muscle. Hepatic steatosis was diagnosed based on enlarged liver size and evidence of diffuse hyper-echogenicity of liver relative to kidneys.

The mean visceral fat was significantly higher in adolescents with increased cIMT (4.8 ±1.6) than in the normal thickness group (3.9 ±1.4). Liver size was also significantly larger in the former group (13.73 ±2.26 versus 12.63 ±2.20) (p = 0.022). After adjusting for other variables, logistic regression demonstrated that glycated hemoglobin (HbA1c) and fatty liver are independent factors affecting cIMT, OR = 1.426 (p < 0.05) and OR = 4.71 (p < 0.05).

In the present study, fatty liver and HbA1c were associated with subclinical atherosclerosis in lean adolescents with T1D.


subclinical atherosclerosis, type 1 diabetes, fatty liver, visceral fat area

Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis 2010; 28: 155-61.
Anderson EL, Howe LD, Jones HE, et al. The prevalence of non-alcoholic fatty liver disease in children and adolescents: a systematic review and meta-analysis. PLoS One 2015; 10: e0140908.
Petit JM, Pedro L, Guiu B, Duvillard L. Type 1 diabetes is not associated with an increased prevalence of hepatic steatosis. Diabet Med 2015; 32: 1648-51.
Bland J, Skordalaki A, Emery JL. Early intimal lesions in the common carotid artery. Cardiovasc Res 1986; 20: 863-8.
Madan SA, John F, Pyrsopoulos N, Pitchumoni CS. Nonalcoholic fatty liver disease and carotid artery atherosclerosis in children and adults: a meta-analysis. Eur J Gastroenterol Hepatol 2015; 27: 1237-48.
Hamaguchi M, Kojima T, Itoh Y, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol 2007; 102: 2708-15.
Palmentieri B, de Sio I, La Mura V, et al. The role of bright liver echo pattern on ultrasound B-mode examination in the diagnosis of liver steatosis. Dig Liver Dis 2006; 38: 485-9.
Atwa HA, Gad AA, El Kelany AM, Rabie HM. Measurement of normative value for carotid artery intima media thickness of healthy male adolescents in Ismailia City. Master Thesis, Suez Canal University Library 2013.
El Ruby MO, Mazen I, Aglan MS, et al. National Project of Standard Growth Curves for Egyptian Children and Adolescents (0–18 y) (1997–2002).
Sun YP, Cai YY, Li HM, Deng SM, Leng RX, Pan HF. Increased carotid intima-media thickness (CIMT) levels in patients with type 1 diabetes mellitus (T1DM): a meta-analysis. J Diab Complications 2015; 29: 724-30.
Shipkova M, Vogeser M, Ramos PA, Verstraete AG. Multi-center analytical evaluation of a novel automated tacrolimus immunoassay. Clin Biochem 2014; 47: 1069-77.
Atwa HA, Shora H. Glycemic control could reverse subclinical atherosclerotic changes and normal adiponectin levels in lean type-1 diabetic children. J Clin Basic Cardiol 2011; 14: 3-6.
Touboul PJ, Hennerici MG, Meairs S, Adams H, Amarenco P. Mannheim carotid intima-media thickness consensus (2004-2006). An update on behalf of the Advisory Board of the 3rd and 4th Watching the Risk Symposium, 13th and 15th European Stroke Conferences, Mannheim, Germany, 2004, and Brussels, Belgium, 2006. Cerebrovasc Dis 2007; 23: 75-80.
Armellini F, Zamboni M, Rigo L, et al. The contribution of sonography to the measurement of intra-abdominal fat. Clin Ultrasound 1990; 18: 563-7.
Eifler RV. The role of ultrasonography in the measurement of subcutaneous and visceral fat and its correlation with hepatic steatosis. Radiol Bras 2013; 46: 273-8.
Konus OL, Ozdemir A, ErbasG, Celik H, Isik S. Normal liver, spleen and kidney dimensions in neonates, infants and children: evaluation with sonography. Am J Roentgenol 1998; 171: 1693-8.
Jarvisalo MJ, Jartti L, Nanto-Salonen K, et al. Increased aortic intima-media thickness a marker of preclinical atherosclerosis in high-risk children. Circulation 2001; 104: 2943-7.
Crouse JR, Tang R, Espeland MA, Terry JG, Morgan T, Mercuri M. Associations of extracranial carotid atherosclerosis progression with coronary status and risk factors in patients with and without coronary artery disease. Circulation 2002; 106: 2061-6.
Espeland MA, Craven TE, Riley WA, Corson J, Romont A, Furberg CD. Reliability of longitudinal ultrasonographic measurements of carotid intimal-medial thicknesses. Asymptomatic Carotid Artery Progression Study Research Group. Stroke 1996; 27: 480-5.
Katakami N, Kaneto H, Shimomura I. Carotid ultrasonography: a potent tool for better clinical practice in diagnosis of atherosclerosis in diabetic patients. J Diabetes Investig 2014; 5: 3-13.
Schnell O, Cappuccio F, Genovese S, Standl E, Valensi P, Ceriello A. Type 1 diabetes and cardiovascular disease. Cardiovasc Diabetol 2013; 12: 156.
Mantovani A, Ballestri S, Lonardo A, Targher G. Cardiovascular disease and myocardial abnormalities in nonalcoholic fatty liver disease. Dig Dis Sci 2016; 61: 1246-67.
Koivisto VA, Stevens LK, Mattock M, et al. Cardiovascular disease and its risk factors in IDDM in Europe. Diabetes Care 1996; 9: 689-97.
Paucillo P, Lannuzzi A, Sartorio R, et al. Increased intima-media thickness of the common carotid artery in hypercholesterolemic children. Arterioscler Thromb Vasc Biol 1994; 14: 1075-9.
Kawamori R, Yamasaki Y, Matsushima H, et al. Prevalence of carotid atherosclerosis in diabetic patients. Ultrasound high-resolution B-mode imaging on carotid arteries. Diabetes Care 1992; 15: 1290-4.
Al-Hussaini AA, Sulaiman N, Al-Zahrani M, Alenazi A, Khan M. Prevalence of liver disease among type 1 diabetic children. J Pediatr Gastroenterol Nutr 2010; 42: 641-9.
Jung UJ, Choi MS. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int J Mol Sci 2014; 15: 6184-223.
El-Koofy NM, Anwar GM, El-Raziky MS, et al. The association of metabolic syndrome, insulin resistance and non-alcoholic fatty liver disease in overweight/ obese children. Saudi J Gastroenterol 2012; 18: 44-9.
Bitsori M, Kafatos A. Dysmetabolic syndrome in childhood and adolescence. Acta Paediatr 2005; 94: 995-1005.
Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 2010; 363: 1341-50.
Day CP, James OF. Steatohepatitis: a tale of two “hits”? Gastroenterology 1998; 114: 842-5.
Guy J, Ogden L, Wadwa RR, et al. Lipid and lipoprotein profiles in youth with and without type 1 diabetes. The SEARCH for Diabetes in Youth Case-Control Study. Diabetes Care 2009; 32: 416-20.
Järvisalo MJ, Putto-Laurila A, Jartti L, et al. Carotid artery intima-media thickness in children with type 1 diabetes. Diabetes 2002; 51: 493-8.
Stein JH, Korcarz CE, Hurst RT, et al. American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Use of carotid ultrasonography to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Endorsed by the Society for Vascular Medicine. J Am Soc Echocardiogr 2008; 21: 93-111.
Lee EJ, Kim HJ, Bae JM, et al. Relevance of common carotid intima-media thickness and carotid plaque as risk factors for ischemic stroke in patients with type 2 diabetes mellitus. AJNR Am J Neuroradiol 2007; 28: 916-9.
Fracanzani AL, Burdick L, Raselli S, et al. Carotid artery intima-media thickness in nonalcoholic fatty disease. Am J Med 2008; 121: 72-8.
Schwimmer JB, Pardee PE, Lavine JE, Blumkin AK, Cook S. Cardiovascular risk factors and the metabolic syndrome in pediatric nonalcoholic fatty liver disease. Circulation 2008; 118: 277-83.
Järvisalo MJ, Raitakari M, Toikka JO, et al. Carotid artery intima-media thickness in children with type 1 diabetes. Circulation 2004; 109: 1750-5.
Fendler W, Rizzo M, Borowiec M, et al. Less but better: cardioprotective lipid profile of patients with GCK-MODY despite lower HDL cholesterol level. Acta Diabetol 2014; 51: 625-32.
Bhatia LS, Curzen NP, Byrne CD. Nonalcoholic fatty liver disease and vascular risk. Curr Opin Cardiol 2012; 27: 420-8.
Atabek ME, Pirgon O, Kivrak AS. Evidence for association between insulin resistance and premature carotid atherosclerosis in children obesity. Pediatr Res 2007; 61: 345-9.
Katsiki N, Athyros VG, Mikhailidis DP. Abnormal peri-organ or intra-organ fat (APIFat) deposition: an underestimated predictor of vascular risk? Curr Vasc Pharmacol 2016; 14: 432-41.
Stepien M, Stepien A, Banach M, et al. New obesity indices and adipokines in normotensive patients and patients with hypertension: comparative pilot analysis. Angiology 2014; 65: 333-42.
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