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Visceral adiposity and subclinical atherosclerosis in healthy young men ab
c
b
b
Gennaro Clemente , Marcello Mancini , Rosalba Giacco , Antonietta Tornatore , Monica d
e
Ragucci & Gabriele Riccardi a
IRPPS – Institute for Research on Population and Social Policies of National Research Council, Penta di Fisciano (SA), Italy, b
ISA Institute of Food Science of National Research Council, Avellino, Italy,
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Institute of Biostructures and Bioimaging, National Research Council, Naples, Italy,
d
Department of Advanced Biomedical Sciences, University “Federico II”, Naples, Italy, and
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Department of Clinical Medicine and Surgery, Medical School University “Federico II” Naples, Italy Published online: 02 Jun 2015.
To cite this article: Gennaro Clemente, Marcello Mancini, Rosalba Giacco, Antonietta Tornatore, Monica Ragucci & Gabriele Riccardi (2015) Visceral adiposity and subclinical atherosclerosis in healthy young men, International Journal of Food Sciences and Nutrition, 66:4, 466-470 To link to this article: http://dx.doi.org/10.3109/09637486.2015.1042845
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http://informahealthcare.com/ijf ISSN: 0963-7486 (print), 1465-3478 (electronic) Int J Food Sci Nutr, 2015; 66(4): 466–470 ! 2015 Informa UK Ltd. DOI: 10.3109/09637486.2015.1042845
STUDIES IN HUMANS
Visceral adiposity and subclinical atherosclerosis in healthy young men Gennaro Clemente1,2, Marcello Mancini3, Rosalba Giacco2, Antonietta Tornatore2, Monica Ragucci4*, and Gabriele Riccardi5 IRPPS – Institute for Research on Population and Social Policies of National Research Council, Penta di Fisciano (SA), Italy, 2ISA Institute of Food Science of National Research Council, Avellino, Italy, 3Institute of Biostructures and Bioimaging, National Research Council, Naples, Italy, 4 Department of Advanced Biomedical Sciences, University ‘‘Federico II’’, Naples, Italy, and 5Department of Clinical Medicine and Surgery, Medical School University ‘‘Federico II’’ Naples, Italy
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Abstract
Keywords
Background: Atherosclerosis begins in childhood and develops silently for decades before clinical events such as myocardial infarction or stroke occur. Only few studies have evaluated the relationship between CVD risk factors and carotid artery Intimal Media Thickness (IMT) in young asymptomatic people. Aim: The aim of this study is to investigate risk factors for cardiovascular disease associated with higher Carotid Intimal Media Thickness (IMT) in healthy young subjects. Methods: A cohort of 106 healthy young men, mean age 21 ± 2 years (mean ± SD), BMI 24.4 ± 2.8 (kg/m2), on military duty, participated in this cross-sectional study. Waist circumference, carotid intima–media thickness (IMT), blood pressure, and plasma concentrations of relevant metabolic parameters were measured at fasting. Smoking and habitual dietary patterns were evaluated by a semiquantitative questionnaire. Results: The population was divided into two groups on the basis of IMT values: the lowest three quartiles versus the highest quartile (cut-off value ¼ 0.7 mm). BMI, waist circumference, systolic (SBP), and diastolic (DBP) blood pressure were significantly higher in the group with higher IMT (p ¼ 0.02). All other variables, including dietary parameters and smoking, were similar in the two groups. Data analysis showed that IMT values correlated positively with SBP (r ¼ 0.22; p ¼ 0.025), DBP (r ¼ 0.27; p ¼ 0.005), waist circumference (r ¼ 0.29; p ¼ 0.002), and fat mass (r ¼ 0.24; p ¼ 0.01), and negatively with kcal/kg of body weight (r ¼ 0.220.22; p ¼ 0.022) – an indirect marker of physical activity. Based on multiple regression analysis, waist circumference and DBP were the only variables independently associated with IMT (p ¼ 0.029). Conclusions: In a non-selected sample of healthy young adult males, a larger waist circumference and a higher diastolic blood pressure – albeit within normal values – are the only parameters independently associated with higher IMT.
Atherosclerosis, nutrition, obesity
Introduction Atherosclerosis begins in childhood and develops silently for decades before clinical events such as myocardial infarction or stroke occur (PDAY Research Group, 1990). Autopsy studies in children and adolescents have confirmed the presence of preclinical atherosclerotic lesions, showing the association of the latter with antemortem vascular risk factors (McGill, 2000; Short, 2009). In asymptomatic middle-aged adults, the metabolic syndrome is associated with accelerated atherosclerosis (Burke, 2006; Herouvi, 2013). Although several studies have associated the presence of risk factors for atherosclerosis with subclinical atherosclerosis in younger adults (Johnson et al., 2007; Tzou, 2005) a population that is becoming increasingly more overweight only few studies have specifically evaluated the
*These authors contributed equally to this work. Correspondence: Dr. Gennaro Clemente, IRPPS – ISA Institute for Research on Population and Social Policies of National Research Council, via V. Emanuele 9/11, 84080 Penta di Fisciano (SA), Italy. Tel: +39 089 891850/1. Fax: +39 089 958365. E-mail: [email protected]
History Received 18 December 2014 Revised 19 March 2015 Accepted 16 April 2015 Published online 28 May 2015
relationship between overweight or abdominal circumference and carotid artery Intimal Media Thickness (IMT) (Davis Patricia et al., 2001; Raikatari et al., 2003; Simon et al., 2010). The evidence of an association between subclinical and potentially reversible vascular disease in young adults and visceral adiposity would emphasize the need for heightened awareness and early prevention of this condition and related comorbidities. The attractive features of IMT measurement as a non-invasive measure of atherosclerosis are that it is safe, relatively inexpensive, does not require exposure to radiation, and is highly reproducible. Moreover, IMT measurement is predictive of future risk for myocardial infarction (MI) and stroke and correlates with vascular risk factors (Burke et al., 1995; Salonen & Salonen, 1991; Simon et al., 2010) in large prospective trials. In the Atherosclerosis Risk in Communities (ARIC) study, a large population aged 45–70 years with no history of coronary heart disease was followed for 4–7 years. The authors found that hazard rate ratios for myocardial infarction or coronary heart disease deaths for the highest versus the lowest IMT tertile were 6.69 for women and 2.88 for men (Chambless et al., 1997). The Cardiovascular Health Study (CHS) evaluated individuals older
DOI: 10.3109/09637486.2015.1042845
than 65 years without clinically apparent coronary heart disease for a median of 6.2 years. Those in the highest IMT quintile had a 3.87 relative risk of MI and stroke compared with those in the lowest quintile. To the best of our knowledge, no such studies have been performed in younger populations; therefore, setting an absolute value as threshold for abnormal IMT using data derived from large population studies, without considering age, would underestimate the risk of CV events in younger populations (Pignoli, 1984; Riley et al., 1992). Against this background, the aim of this study was to investigate traditional risk factors for Cardiovascular Disease associated with a higher Carotid Intimal Media Thickness in healthy young subjects.
Methods
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Participants We screened a cohort of healthy young men comprising all new comers in the first 3 months of the year to the military basis of Avellino (Southern Italy) to fulfil their military duties. Based on the inclusion criteria (age between 18 and 30 years, total cholesterol 220 mg/dl, triglyceride 150 mg/dl, plasma glucose 100 mg/dl, BP140/90 mmHg, and waist circumference 102 cm), 120 healthy young men were eligible for the study and consecutively enrolled within a 6-month period. The overall participation rate was 88%, leading to a cohort of 106 participants. The study protocol was formally approval by the Ethics Committee of the Army Health Service based in Avellino (232nd RGT), which complies with the Guidelines of the General Ethics committee in Rome (COMITATO DI BIOETICA DEL POLICLINICO MILITARE CELIO DI ROMA) and verbal informed consent was obtained from each participant before the beginning of the study. Study design and methods In this cross-sectional study, all participants were scheduled to attend the Human Nutrition Unit of the Institute of Food Science of the Italian National Research Council at 08.00 a.m. after a 12–14 h fast. Blood samples were taken to measure glucose, cholesterol, triglycerides, and FFA plasma concentrations. Anthropometric parameters, body composition, blood pressure, and IMT were measured. On the same morning, nutritional and lifestyle habits were investigated by a food frequency questionnaire (FFQ).
Visceral adiposity and IMT in healthy young men
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Body composition A Bioelectrical Impedance Analyzer (STA-BIA AKERN, Akern, Italy) was used for the measurement of Resistance (R) and Reactance (X) of body tissue; these parameters, together with body weight and height, were used to calculate each participants Fat Free body Mass (FFM) according to Kotler’s equation (Lukaski et al., 1986). Fat mass (FM) was calculated subtracting FFM from body weight. The measurements were performed according to a standard protocol in the morning of the experiment after a 12-h fast. Blood pressure Blood pressure was measured using a mercury sphygmomanometer with the participants in the sitting position after a 5-min rest. Systolic blood pressure (SBP) was determined by the onset of the ‘‘tapping’’ Korotkoff sounds. Diastolic blood pressure (DBP) was measured at the disappearance of the Korotkoff sounds. Blood pressure was measured three times at 5 min intervals and the mean value was calculated. Carotid intimal medial thickness To measure the carotid intimal medial thickness (IMT), a B-mode ultrasound examination of the common carotid artery, carotid bifurcation, and internal carotid artery of the left and right side was performed by a single sonographer using a 12 MHz linear array transducer with ultrasound system ATL-HDI 3000 (ATL Ultrasound, Bothell, WA), according to a standardized scanning protocol. The study protocol involved scanning of the distal 1 cm of the near and far walls of the common carotid arteries. The beginning of the dilatation and the crest of the bifurcation were used as anatomical landmarks to identify the other segments. In each examination, the sonographer used different longitudinal scanning angles (anterior, lateral, and posterior) to identify the greatest IMT in the anterior (near) and posterior (far) walls of the carotid artery. The maximum IMT of the near and far wall and the mean value of the four maximum thicknesses (two from the left and two from the right) were used as representative values for each individual. These scans were carried out with the subjects laying supine. The axial resolution of the system was 0.1 mm. IMT was measured as the distance between the leading edge of the first echogenic line of the far wall (lumen intima interface) and the leading edge of the second echogenic line (media adventitia interface) (Heiss et al., 1991; Lorenz et al., 2012). For the near wall, the distance between the trailing edge of the first and the second echogenic lines provides the near wall IMT (Pignoli, 1984).
Blood analytes Plasma concentrations of glucose, total cholesterol, HDL-cholesterol, and triacylglycerol were measured by enzymatic–colorimetric methods (Roche Molecular Biochemicals, Mannheim, Germany) on a Cobas Mira Plus autoanalyser (ABX Diagnostics, Montpellier, France). The LDL cholesterol concentration was calculated using Friedwald’s formula.
Nutritional and lifestyle questionnaire Nutritional and lifestyle habits were investigated in all individuals by a food frequency questionnaire validated in a representative sample of healthy people from the same geographical region (Food questionnaire for epidemiological studies on large cohorts for use in Italy (Trevisan et al., 1992)).
Antropometric parameters
Statistical analysis
Participants’ height was assessed using a stadiometer and weight measured to the nearest tenth of a kilo using the SECA digital body weight scale. Weight and height measurements were used to calculate the participant’s Body Mass Index (BMI). Waist circumference was evaluated, at the end of a normal expiration with a measuring tape placed in a horizontal plane around the abdomen, at the level of the iliac crest; the value was approximated to the nearest centimetre.
Statistical analysis was conducted using the SPSS statistical package (ver. 18.0; SPSS Inc., Chicago, IL). Normal distribution was tested by Shapiro’s test. Continuous data were expressed as means ± SD. The average IMT value between left and right carotid arteries values was calculated. The population was divided into two groups (the lowest three quartiles versus the highest quartile) on the basis of IMT values. The cut-off between the third and the
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Int J Food Sci Nutr, 2015; 66(4): 466–470
Table 1. Characteristics of the study participants (M ± SD). Gender Number Smokers no. (%) Age (years) Body Mass Index (kg/m2) Waist circumference (cm) Glucose (mg/dl) Cholesterol (mg/dl) Triglycerides (mg/dl) HDL-cholesterol (mg/dl) LDL-cholesterol (mg/dl) SBP (mmHg) DBP (mmHg)
Table 3. Composition of the habitual diet of the study participants according to IMT value. Males 106 61 (57) 21 ± 2 24.4 ± 2.8 85.8 ± 8.2 81 ± 8 158 ± 31 66 ± 27 41 ± 8 106 ± 29 117 ± 9 72 ± 8
Table 2. Cardiovascular risk factors in individuals in the highest quartile of IMT as compared with the remaining population. Intima–media thickness*
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50.7 mm (n ¼ 79)
Age (years) BMI (kg/m2) Waist circumference (cm) Fat mass (kg) Energy intake/BW (kcal/kg) Cholesterol (mg/dl) Triglycerides (mg/dl) HDL-Chol (mg/dl) LDL-Chol (mg/dl) Glucose (mg/dl) SBP (mmHg) DBP (mmHg) Smoking (cigarettes no./d)
0.7 mm (n ¼ 27) Mean
SD
Mean
SD
p
21.3 24 84.7 15.1 43.8 159.8 64.2 41.7 107.4 81.4 115.9 71 12.2
2 2 7 4 13 32 23 7 30 8 7 8 7
21.4 25.4 89 16.9 40.8 152.9 70 38.7 102.5 81.5 119.7 74.6 11.5
2 3 10 5 14 27 34 7 25 8 7 10 5
0.95 0.029 0.019 0.083 0.324 0.31 0.33 0.09 0.45 0.95 0.043 0.037 0.789
Bold values indicate a p50.05. *At the bifurcation of carotid artery. t-test for unpaired data.
fourth quartile was 0.7 mm. Statistically significant differences between the two groups were evaluated by the unpaired Student t-test. Correlations between variables and IMT were assessed by Spearman’s correlation coefficients. A multiple linear regression analysis was performed between IMT (considered as the dependent variable) and variables significantly correlated with IMT according to the univariate analysis. A p-level 50.05 (two tails) was considered statistically significant.
Results All participants showed normal values of fasting plasma glucose and lipid concentrations, normal blood pressure levels, and had a waist circumference below 5102 cm (Table 1). Fifty-seven percent of the participants was current smokers (Table 1). As expected, the echographic evaluation of the carotid artery failed to find any clinically significant abnormality in any of the participants (data not shown). The population was divided into two groups based on IMT values: the lowest three quartiles versus the highest quartile (cut-off value ¼ 0.7 mm). BMI, waist circumference, and SBP and DBP were significantly higher in the group with higher IMT (Table 2). All other variables were similar in the two groups (Table 2) as was their diet composition (Table 3). However, the percentage of smokers between the two groups was slightly but not significantly lower in the group with higher IMT compared with the group with lower IMT (44% versus 62%), with no difference in the number of cigarettes smoked per day between
Energy (kcal/d) Protein (g/d) Carbohydrates (g/d) Total lipids (g/d) Saturated fat (g/d) Monounsaturated (g/d) Polyunsaturated (g/d) Cholesterol (mg/d) Dietary fiber (g/d)
IMT 50.7 mm (n ¼ 79)
IMT 0.7 mm (n ¼ 27)
3098 ± 745 121 ± 31 (15.9%) 461 ± 120 (56.4%) 93 ± 25 (27.5%) 36 ± 11 (10.4%) 38 ± 10 (11.3%) 13 ± 3 (3.8%) 481 ± 165 30 ± 8
2993 ± 721 118 ± 29 (16.0%) 445 ± 120 (56.4%) 89 ± 22 (27.4%) 33 ± 8 (10.2%) 36 ± 9 (11.1%) 13 ± 4 (4.1%) 455 ± 136 31 ± 9
the two groups (Table 2). Data analysis showed that IMT values correlated positively with SBP (r ¼ 0.22; p ¼ 0.025), DBP (r ¼ 0.27; p ¼ 0.005), waist circumference (r ¼ 0.29; p ¼ 0.002), and fat mass (r ¼ 0.24; p ¼ 0.01), and negatively with kcal/kg of body weight (r ¼ 0.22; p ¼ 0.022) – an indirect marker of physical activity (Figure 1) (Melzer et al., 2005). Multiple linear regression analysis demonstrated that in this population waist circumference and DBP were the only variables independently associated with IMT (Table 4).
Discussion Measurement of carotid IMT has gained acceptance in older adults as a non-invasive, inexpensive method to assess extent and severity of preclinical atherosclerosis. Several pieces of evidence support the validity of this measurement (Fernandes et al., 2006; Graner et al., 2006). Carotid IMT evaluated with ultrasonography correlates well with arteriosclerosis present in other arterial districts, namely in coronary vessels (Tsivgoulis et al., 2006; Van der Meer et al., 2004). Increased carotid IMT is significantly related to known cardiovascular risk factors and to the presence of carotid plaques a more advanced type of atherosclerotic lesion. Finally, carotid IMT is not only associated with stroke, coronary artery disease and peripheral vascular disease but also a reliable predictor of incident cardiovascular disease events (Oren et al., 2003; Peppa-Patrikiou et al., 1998). So far, there are limited data concerning carotid IMT in young and middle-aged adults (Burke et al., 1995; Vos et al., 2003). Our study shows that abdominal waist and DBP are the strongest predictors of higher carotid IMT in young adult males, since no other risk factors remained significantly associated with IMT after performing multivariate analysis. At first sight, it may be surprising that plasma cholesterol levels and smoking habits were not associated with IMT in our study. However, it should be underlined that our study population was selected based on perfectly normal plasma glucose, cholesterol, and triglyceride levels. Moreover, there is clear evidence that the metabolic syndrome increases the risk of cardiovascular alterations already at an early age (Takami et al., 2001; Tzou et al., 2005). However, none of the young men who participated in our study presented anthropometric and/or metabolic parameters that meet the diagnostic criteria for the metabolic syndrome according to the ATP III and AHA criteria set in 2005. Previous studies report that IMT is positively related to the prevalence of smokers and to the number of cigarettes smoked per day (Baldassarre et al., 2009). This finding was not confirmed in our study likely due to the young age of our participants. In fact, the literature is concordant in showing that the ill effects of smoking on the arterial wall are very seldom seen in very young subjects while they become evident at a later stage (Stamler et al., 2000).
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Figure 1. Spearman’s correlation analysis of measured values of intima–media thickness of the carotid bifurcation and other relevant parameters. SBP: r ¼ 0.218, p50.025 (a); DBP: r ¼ 0.27, p ¼ 0.005 (b); kcal/kg body weight: r ¼ 0.22, p ¼ 0.022 (c); waist circumference: r ¼ 0.29, p ¼ 0.0022 (d); fat mass: r ¼ 0.24, p ¼ 0.01 (e).
Table 4. Multiple linear regression independently associated with IMT. B
SE
analysis
p
of
T
the
f
variables
p
Waist circumference (cm) 0.002 0.001 0.012 2.554 7.60 50.001 DBP (mmHg) 0.002 0.001 0.034 2.146 Variables entered in the model: waist circumference, diastolic blood pressure, systolic blood pressure, BMI, fat mass and number of cigarettes smoked.
Case–control studies of children and young adults demonstrate that familial hypercholesterolemia and borderline hypertension are associated with grater IMT (Takami et al., 2001; Zhang et al., 2013). Young adults with diabetes also present with higher carotid IMT than controls (Jarvisalo et al., 2002). However, to our knowledge, this is the first study demonstrating an association between higher IMT and visceral adiposity, independently of major cardiovascular risk factors in healthy young men. This information emphasizes the need to start all lifestyle measures able to reduce/prevent abdominal obesity as early as possible. As a matter of fact already in the second decade of life, the presence of this condition is associated with preclinical markers of atherosclerosis which may later on result in clinical events. The main limitation of this study is its observational design, based on a cross-sectional evaluation. Therefore, we can only detect associations between study variables, whereas
we are unable to infer any causality. Indeed, the results of this study need to be reproduced in longitudinal studies and, possibly, in intervention trials. Other limitations are the relatively small sample size and the restriction of the observation to the male gender, which does not allow us to extrapolate our results to the female population. The main strength of our study is the evaluation of IMT and associated risk markers in a young healthy population. This is relevant to establish whether the same cardiovascular risk factors are operative in young adults as in older ones, and to decide targets for an early prevention of cardiovascular diseases in adolescents and young adults.
Conclusions In conclusion, this study shows that in a non-selected sample of healthy young adult males, a larger waist circumference and a higher diastolic blood pressure – albeit within normal values – are associated with increased carotid intima–media thickness. The results of this study highlight the potential usefulness of the IMT measurement in clinical practice also in people aged less than 30 years in order to identify people at increased cardiovascular risk. Moreover, they emphasize the need to start lifestyle interventions to prevent cardiovascular diseases already in adolescents and young adults.
Acknowledgements The authors thank Mrs. Rosanna Scala for the language editing; Mrs. Anna Maria Palumbo for the statistical analysis.
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Declaration of interest The authors report that they have no conflicts of interest.
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References Baldassarre D, Castelnuovo S, Frigerio B, Amato M, Werba JP, De Jong A, Ravani AL, et al. 2009. Effects of timing and extent of smoking, type of cigarettes, and concomitant risk factors on the association between smoking and subclinical atherosclerosis. Stroke 40:1991–1998. Burke GL, Evans GW, Riley WA, Sharrett AR, Howard G, Barnes RW, Rosamond W, et al. 1995. Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) study. Stroke 26: 386–391. Burke V. 2006. Obesity in childhood and cardiovascular risk. Clin Exp Pharmacol Physiol 33:831–837. Chambless LE, Heiss G, Folsom AR, Rosamond W, Szklo M, Sharrett AR, Clegg LX. 1997. 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 146:483–494. Davis Patricia H, Dawson Jeffrey D, Riley Ward A, Lauer Ronald M. 2001. Carotid intimal-medial thickness is related to cardiovascular risk factors measured from childhood through middle age: the Muscatine study. Circulation 104:2815–2819. Fernandes VR, Polak JF, Evdardsen T, Carvalho B, Gomes A, Bluemke DA, Nasir K, et al. 2006. Subclinical atherosclerosis and incipient regional myocardial dysfunction in asymptomatic individuals: the Multi-Ethnic Study of Atherosclerosis (MESA). J Am Coll Cardiol 47:2420–2428. Graner M, Varpula M, Kahri J, Salonen RM, Nyysso¨nen K, Nieminen MS, Taskinen MR, Syva¨nne M. 2006. Association of carotid intima– media thickness with angiographic severity and extent of coronary artery disease. Am J Cardiol 97:624–629. Heiss G, Sharrett AR, Barnes R, Chambless LE, Szklo M, Alzola C. 1991. Carotid atherosclerosis measured by B-mode ultrasound in populations: associations with cardiovascular risk factors in ARIC study. Am J Epidemiol 134:250–256. Herouvi D, Karanasios E, Karayianni C, Karavanaki K. 2013. Cardiovascular disease in childhood: the role of obesity. Eur J Pediatr 172:721–732. Jarvisalo MJ, Putto-Laurila A, Jartti L, Lehtima¨ki T, Solakivi T, Ro¨nnemaa T, Raitakari OT. 2002. Carotid artery intima–media thickness in children with type 1 diabetes. Diabetes 51:493–498. Johnson HM, Douglas PS, Srinivasan SR, Bond MG, Tang R, Li S, Chen W, et al. 2007. Predictors of carotid intima–media thickness progression in young adults: the Bogalusa Heart Study. Stroke 38: 900–905. Lorenz MW, Polak JF, Kavousi M, Mathiesen EB, Vo¨lzke H, Tuomainen TP, Sander D, et al., PROG-IMT Study Group. 2012. Carotid intima–media thickness progression to predict cardiovascular events in the general population (the PROG-IMT collaborative project): a meta-analysis of individual participant data. Lancet 379: 2053–2062. Lukaski HC, Bolonchuk WW, Hall CB, Siders WA. 1986. Validation of tetrapolar bioelectrical impedence method to assess human body composition. J Appl Physiol 60:1327–1332. McGill Jr HC, McMahan CA, Herderick EE, Tracy RE, Malcom GT, Zieske AW, Strong JP for the PDAY Research Group. 2000. Effects of coronary research disease risk factors on atherosclerosis of selected regions of aorta and right coronary artery. Arterioscler Thromb Vasc Biol 20:836–845.
Int J Food Sci Nutr, 2015; 66(4): 466–470
Melzer K, Kayser B, Saris WH, Pichard C. 2005. Effects of physical activity on food intake. Clin Nutr 24:885–895. Oren A, Vos LE, Uiterwaal CS, Grobbee DE, Bots ML. 2003. Cardiovascular risk factors and increased carotid intima–media thickness in healthy young adults: the ARYA Study. Arch Intern Med 163: 1787–1792. PDAY Research Group. 1990. Relationship of atherosclerosis in young men to serum lipoprotein cholesterol concentrations and smoking: a preliminary report from the. JAMA 264:3018–3024. Peppa-Patrikiou M, Scordili M, Antoniu A, Giannaki M, Dracopoulou M, Dacou-Voutetakis C. 1998. Carotid atherosclerosis in adolescents and young adults with IDDM. Diabetes Care 21:1004–1007. Pignoli P. 1984. Ultrasound B-mode imaging for arterial wall thickness measurement. Atheroscler Rev 12:177–184. Raikatari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Ma¨kiTorkko N, Ja¨rvisalo MJ, et al. 2003. Cardiovascular risk factors in childhood and carotid artery intima–media thickness in adulthood. JAMA 290:2277–2283. Riley WA, Barnes RW, Applegate WB, Dempsey R, Hartwell T, Davis VG, Bond MG, Furberg CD. 1992. Reproducibility of non-invasive ultrasonic measurement of carotid atherosclerosis: the Asymptomatic Carotid Artery Plaque Study. Stroke 23: 1062–1068. Salonen JT, Salonen R. 1991. Ultrasonographically assessed carotid morphology and the risk of coronary heart disease. Arterioscler Thromb 11:1245–1249. Short KR, Blackett PR, Gardner AW, Copeland KC. 2009. Vascular health in children and adolescents: effects of obesity and diabetes. Vasc Health Risk Manag 5:973–990. Simon A, Megnien JL, Chironi G. 2010. The value of carotid intima– media thickness for predicting cardiovascular risk. Arterioscler Thromb Vasc Biol 30:182–185. Stamler J, Daviglus ML, Garside DB, Greenland P, Neaton JD. 2000. Relation of baseline serum cholesterol levels in 3 large cohorts of younger men to long-term coronary, cardiovascular, and all cause mortality and to longevity. JAMA 284:311–318. Takami R, Takeda N, Hayashi M, Sasaki A, Kawachi S, Yoshino K, Takami K, et al. 2001. Body fatness and fat distribution as predictors of metabolic abnormalities and early carotid atherosclerosis. Diabetes Care 24:1248–1252. Trevisan M, Krogh V, Ferro-Luzzi A, Riccardi G, Freudenheim J, Sette S, Scaccini C. 1992. Food questionnaire for epidemiological studies on large cohorts for use in Italy. Ann Ist Supe Sanita` 28:397–401. Tsivgoulis G, Vemmos K, Papamichael C, Spengos K, Manios E, Stamatelopoulos K, Vassilopoulos D, Zakopoulos N. 2006. Common carotid artery intima–media thickness and the risk of stroke recurrence. Stroke 37:1913–1916. Tzou WS, Douglas PS, Srinivasan SR, Bond MG, Tang R, Chen W, et al. 2005. Increased subclinical atherosclerosis in young adults with metabolic syndrome. J Am Coll Cardiol 46:457–463. Van der Meer IM, Bots ML, Hofman A, del Sol AI, van der Kuip DA, Witteman JC. 2004. Predictive value of noninvasive measures of atherosclerosis for incident myocardial infarction: the Rotterdam Study. Circulation 109:1089–1094. Vos LE, Oren A, Uiterwaal CS, Gorissen WH, Grobbee DE, Bots ML. 2003. Adolescent blood pressure and blood pressure tracking into young adulthood are related to subclinical atherosclerosis: the Atherosclerosis Risk in Young Adults (ARYA) study. Am J Hypertension 16:549–555. Zhang ZQ, Deng J, He LP, Ling WH, Su YX, Chen YM. 2013. Comparison of various anthropometric and body fat indices in identifying cardiometabolic disturbances in Chinese men and women. PLoS One 8:e70893.
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Visceral adiposity and subclinical atherosclerosis in healthy young men ab
c
b
b
Gennaro Clemente , Marcello Mancini , Rosalba Giacco , Antonietta Tornatore , Monica d
e
Ragucci & Gabriele Riccardi a
IRPPS – Institute for Research on Population and Social Policies of National Research Council, Penta di Fisciano (SA), Italy, b
ISA Institute of Food Science of National Research Council, Avellino, Italy,
c
Institute of Biostructures and Bioimaging, National Research Council, Naples, Italy,
d
Department of Advanced Biomedical Sciences, University “Federico II”, Naples, Italy, and
e
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Department of Clinical Medicine and Surgery, Medical School University “Federico II” Naples, Italy Published online: 02 Jun 2015.
To cite this article: Gennaro Clemente, Marcello Mancini, Rosalba Giacco, Antonietta Tornatore, Monica Ragucci & Gabriele Riccardi (2015) Visceral adiposity and subclinical atherosclerosis in healthy young men, International Journal of Food Sciences and Nutrition, 66:4, 466-470 To link to this article: http://dx.doi.org/10.3109/09637486.2015.1042845
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http://informahealthcare.com/ijf ISSN: 0963-7486 (print), 1465-3478 (electronic) Int J Food Sci Nutr, 2015; 66(4): 466–470 ! 2015 Informa UK Ltd. DOI: 10.3109/09637486.2015.1042845
STUDIES IN HUMANS
Visceral adiposity and subclinical atherosclerosis in healthy young men Gennaro Clemente1,2, Marcello Mancini3, Rosalba Giacco2, Antonietta Tornatore2, Monica Ragucci4*, and Gabriele Riccardi5 IRPPS – Institute for Research on Population and Social Policies of National Research Council, Penta di Fisciano (SA), Italy, 2ISA Institute of Food Science of National Research Council, Avellino, Italy, 3Institute of Biostructures and Bioimaging, National Research Council, Naples, Italy, 4 Department of Advanced Biomedical Sciences, University ‘‘Federico II’’, Naples, Italy, and 5Department of Clinical Medicine and Surgery, Medical School University ‘‘Federico II’’ Naples, Italy
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Abstract
Keywords
Background: Atherosclerosis begins in childhood and develops silently for decades before clinical events such as myocardial infarction or stroke occur. Only few studies have evaluated the relationship between CVD risk factors and carotid artery Intimal Media Thickness (IMT) in young asymptomatic people. Aim: The aim of this study is to investigate risk factors for cardiovascular disease associated with higher Carotid Intimal Media Thickness (IMT) in healthy young subjects. Methods: A cohort of 106 healthy young men, mean age 21 ± 2 years (mean ± SD), BMI 24.4 ± 2.8 (kg/m2), on military duty, participated in this cross-sectional study. Waist circumference, carotid intima–media thickness (IMT), blood pressure, and plasma concentrations of relevant metabolic parameters were measured at fasting. Smoking and habitual dietary patterns were evaluated by a semiquantitative questionnaire. Results: The population was divided into two groups on the basis of IMT values: the lowest three quartiles versus the highest quartile (cut-off value ¼ 0.7 mm). BMI, waist circumference, systolic (SBP), and diastolic (DBP) blood pressure were significantly higher in the group with higher IMT (p ¼ 0.02). All other variables, including dietary parameters and smoking, were similar in the two groups. Data analysis showed that IMT values correlated positively with SBP (r ¼ 0.22; p ¼ 0.025), DBP (r ¼ 0.27; p ¼ 0.005), waist circumference (r ¼ 0.29; p ¼ 0.002), and fat mass (r ¼ 0.24; p ¼ 0.01), and negatively with kcal/kg of body weight (r ¼ 0.220.22; p ¼ 0.022) – an indirect marker of physical activity. Based on multiple regression analysis, waist circumference and DBP were the only variables independently associated with IMT (p ¼ 0.029). Conclusions: In a non-selected sample of healthy young adult males, a larger waist circumference and a higher diastolic blood pressure – albeit within normal values – are the only parameters independently associated with higher IMT.
Atherosclerosis, nutrition, obesity
Introduction Atherosclerosis begins in childhood and develops silently for decades before clinical events such as myocardial infarction or stroke occur (PDAY Research Group, 1990). Autopsy studies in children and adolescents have confirmed the presence of preclinical atherosclerotic lesions, showing the association of the latter with antemortem vascular risk factors (McGill, 2000; Short, 2009). In asymptomatic middle-aged adults, the metabolic syndrome is associated with accelerated atherosclerosis (Burke, 2006; Herouvi, 2013). Although several studies have associated the presence of risk factors for atherosclerosis with subclinical atherosclerosis in younger adults (Johnson et al., 2007; Tzou, 2005) a population that is becoming increasingly more overweight only few studies have specifically evaluated the
*These authors contributed equally to this work. Correspondence: Dr. Gennaro Clemente, IRPPS – ISA Institute for Research on Population and Social Policies of National Research Council, via V. Emanuele 9/11, 84080 Penta di Fisciano (SA), Italy. Tel: +39 089 891850/1. Fax: +39 089 958365. E-mail: [email protected]
History Received 18 December 2014 Revised 19 March 2015 Accepted 16 April 2015 Published online 28 May 2015
relationship between overweight or abdominal circumference and carotid artery Intimal Media Thickness (IMT) (Davis Patricia et al., 2001; Raikatari et al., 2003; Simon et al., 2010). The evidence of an association between subclinical and potentially reversible vascular disease in young adults and visceral adiposity would emphasize the need for heightened awareness and early prevention of this condition and related comorbidities. The attractive features of IMT measurement as a non-invasive measure of atherosclerosis are that it is safe, relatively inexpensive, does not require exposure to radiation, and is highly reproducible. Moreover, IMT measurement is predictive of future risk for myocardial infarction (MI) and stroke and correlates with vascular risk factors (Burke et al., 1995; Salonen & Salonen, 1991; Simon et al., 2010) in large prospective trials. In the Atherosclerosis Risk in Communities (ARIC) study, a large population aged 45–70 years with no history of coronary heart disease was followed for 4–7 years. The authors found that hazard rate ratios for myocardial infarction or coronary heart disease deaths for the highest versus the lowest IMT tertile were 6.69 for women and 2.88 for men (Chambless et al., 1997). The Cardiovascular Health Study (CHS) evaluated individuals older
DOI: 10.3109/09637486.2015.1042845
than 65 years without clinically apparent coronary heart disease for a median of 6.2 years. Those in the highest IMT quintile had a 3.87 relative risk of MI and stroke compared with those in the lowest quintile. To the best of our knowledge, no such studies have been performed in younger populations; therefore, setting an absolute value as threshold for abnormal IMT using data derived from large population studies, without considering age, would underestimate the risk of CV events in younger populations (Pignoli, 1984; Riley et al., 1992). Against this background, the aim of this study was to investigate traditional risk factors for Cardiovascular Disease associated with a higher Carotid Intimal Media Thickness in healthy young subjects.
Methods
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Participants We screened a cohort of healthy young men comprising all new comers in the first 3 months of the year to the military basis of Avellino (Southern Italy) to fulfil their military duties. Based on the inclusion criteria (age between 18 and 30 years, total cholesterol 220 mg/dl, triglyceride 150 mg/dl, plasma glucose 100 mg/dl, BP140/90 mmHg, and waist circumference 102 cm), 120 healthy young men were eligible for the study and consecutively enrolled within a 6-month period. The overall participation rate was 88%, leading to a cohort of 106 participants. The study protocol was formally approval by the Ethics Committee of the Army Health Service based in Avellino (232nd RGT), which complies with the Guidelines of the General Ethics committee in Rome (COMITATO DI BIOETICA DEL POLICLINICO MILITARE CELIO DI ROMA) and verbal informed consent was obtained from each participant before the beginning of the study. Study design and methods In this cross-sectional study, all participants were scheduled to attend the Human Nutrition Unit of the Institute of Food Science of the Italian National Research Council at 08.00 a.m. after a 12–14 h fast. Blood samples were taken to measure glucose, cholesterol, triglycerides, and FFA plasma concentrations. Anthropometric parameters, body composition, blood pressure, and IMT were measured. On the same morning, nutritional and lifestyle habits were investigated by a food frequency questionnaire (FFQ).
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Body composition A Bioelectrical Impedance Analyzer (STA-BIA AKERN, Akern, Italy) was used for the measurement of Resistance (R) and Reactance (X) of body tissue; these parameters, together with body weight and height, were used to calculate each participants Fat Free body Mass (FFM) according to Kotler’s equation (Lukaski et al., 1986). Fat mass (FM) was calculated subtracting FFM from body weight. The measurements were performed according to a standard protocol in the morning of the experiment after a 12-h fast. Blood pressure Blood pressure was measured using a mercury sphygmomanometer with the participants in the sitting position after a 5-min rest. Systolic blood pressure (SBP) was determined by the onset of the ‘‘tapping’’ Korotkoff sounds. Diastolic blood pressure (DBP) was measured at the disappearance of the Korotkoff sounds. Blood pressure was measured three times at 5 min intervals and the mean value was calculated. Carotid intimal medial thickness To measure the carotid intimal medial thickness (IMT), a B-mode ultrasound examination of the common carotid artery, carotid bifurcation, and internal carotid artery of the left and right side was performed by a single sonographer using a 12 MHz linear array transducer with ultrasound system ATL-HDI 3000 (ATL Ultrasound, Bothell, WA), according to a standardized scanning protocol. The study protocol involved scanning of the distal 1 cm of the near and far walls of the common carotid arteries. The beginning of the dilatation and the crest of the bifurcation were used as anatomical landmarks to identify the other segments. In each examination, the sonographer used different longitudinal scanning angles (anterior, lateral, and posterior) to identify the greatest IMT in the anterior (near) and posterior (far) walls of the carotid artery. The maximum IMT of the near and far wall and the mean value of the four maximum thicknesses (two from the left and two from the right) were used as representative values for each individual. These scans were carried out with the subjects laying supine. The axial resolution of the system was 0.1 mm. IMT was measured as the distance between the leading edge of the first echogenic line of the far wall (lumen intima interface) and the leading edge of the second echogenic line (media adventitia interface) (Heiss et al., 1991; Lorenz et al., 2012). For the near wall, the distance between the trailing edge of the first and the second echogenic lines provides the near wall IMT (Pignoli, 1984).
Blood analytes Plasma concentrations of glucose, total cholesterol, HDL-cholesterol, and triacylglycerol were measured by enzymatic–colorimetric methods (Roche Molecular Biochemicals, Mannheim, Germany) on a Cobas Mira Plus autoanalyser (ABX Diagnostics, Montpellier, France). The LDL cholesterol concentration was calculated using Friedwald’s formula.
Nutritional and lifestyle questionnaire Nutritional and lifestyle habits were investigated in all individuals by a food frequency questionnaire validated in a representative sample of healthy people from the same geographical region (Food questionnaire for epidemiological studies on large cohorts for use in Italy (Trevisan et al., 1992)).
Antropometric parameters
Statistical analysis
Participants’ height was assessed using a stadiometer and weight measured to the nearest tenth of a kilo using the SECA digital body weight scale. Weight and height measurements were used to calculate the participant’s Body Mass Index (BMI). Waist circumference was evaluated, at the end of a normal expiration with a measuring tape placed in a horizontal plane around the abdomen, at the level of the iliac crest; the value was approximated to the nearest centimetre.
Statistical analysis was conducted using the SPSS statistical package (ver. 18.0; SPSS Inc., Chicago, IL). Normal distribution was tested by Shapiro’s test. Continuous data were expressed as means ± SD. The average IMT value between left and right carotid arteries values was calculated. The population was divided into two groups (the lowest three quartiles versus the highest quartile) on the basis of IMT values. The cut-off between the third and the
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Table 1. Characteristics of the study participants (M ± SD). Gender Number Smokers no. (%) Age (years) Body Mass Index (kg/m2) Waist circumference (cm) Glucose (mg/dl) Cholesterol (mg/dl) Triglycerides (mg/dl) HDL-cholesterol (mg/dl) LDL-cholesterol (mg/dl) SBP (mmHg) DBP (mmHg)
Table 3. Composition of the habitual diet of the study participants according to IMT value. Males 106 61 (57) 21 ± 2 24.4 ± 2.8 85.8 ± 8.2 81 ± 8 158 ± 31 66 ± 27 41 ± 8 106 ± 29 117 ± 9 72 ± 8
Table 2. Cardiovascular risk factors in individuals in the highest quartile of IMT as compared with the remaining population. Intima–media thickness*
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50.7 mm (n ¼ 79)
Age (years) BMI (kg/m2) Waist circumference (cm) Fat mass (kg) Energy intake/BW (kcal/kg) Cholesterol (mg/dl) Triglycerides (mg/dl) HDL-Chol (mg/dl) LDL-Chol (mg/dl) Glucose (mg/dl) SBP (mmHg) DBP (mmHg) Smoking (cigarettes no./d)
0.7 mm (n ¼ 27) Mean
SD
Mean
SD
p
21.3 24 84.7 15.1 43.8 159.8 64.2 41.7 107.4 81.4 115.9 71 12.2
2 2 7 4 13 32 23 7 30 8 7 8 7
21.4 25.4 89 16.9 40.8 152.9 70 38.7 102.5 81.5 119.7 74.6 11.5
2 3 10 5 14 27 34 7 25 8 7 10 5
0.95 0.029 0.019 0.083 0.324 0.31 0.33 0.09 0.45 0.95 0.043 0.037 0.789
Bold values indicate a p50.05. *At the bifurcation of carotid artery. t-test for unpaired data.
fourth quartile was 0.7 mm. Statistically significant differences between the two groups were evaluated by the unpaired Student t-test. Correlations between variables and IMT were assessed by Spearman’s correlation coefficients. A multiple linear regression analysis was performed between IMT (considered as the dependent variable) and variables significantly correlated with IMT according to the univariate analysis. A p-level 50.05 (two tails) was considered statistically significant.
Results All participants showed normal values of fasting plasma glucose and lipid concentrations, normal blood pressure levels, and had a waist circumference below 5102 cm (Table 1). Fifty-seven percent of the participants was current smokers (Table 1). As expected, the echographic evaluation of the carotid artery failed to find any clinically significant abnormality in any of the participants (data not shown). The population was divided into two groups based on IMT values: the lowest three quartiles versus the highest quartile (cut-off value ¼ 0.7 mm). BMI, waist circumference, and SBP and DBP were significantly higher in the group with higher IMT (Table 2). All other variables were similar in the two groups (Table 2) as was their diet composition (Table 3). However, the percentage of smokers between the two groups was slightly but not significantly lower in the group with higher IMT compared with the group with lower IMT (44% versus 62%), with no difference in the number of cigarettes smoked per day between
Energy (kcal/d) Protein (g/d) Carbohydrates (g/d) Total lipids (g/d) Saturated fat (g/d) Monounsaturated (g/d) Polyunsaturated (g/d) Cholesterol (mg/d) Dietary fiber (g/d)
IMT 50.7 mm (n ¼ 79)
IMT 0.7 mm (n ¼ 27)
3098 ± 745 121 ± 31 (15.9%) 461 ± 120 (56.4%) 93 ± 25 (27.5%) 36 ± 11 (10.4%) 38 ± 10 (11.3%) 13 ± 3 (3.8%) 481 ± 165 30 ± 8
2993 ± 721 118 ± 29 (16.0%) 445 ± 120 (56.4%) 89 ± 22 (27.4%) 33 ± 8 (10.2%) 36 ± 9 (11.1%) 13 ± 4 (4.1%) 455 ± 136 31 ± 9
the two groups (Table 2). Data analysis showed that IMT values correlated positively with SBP (r ¼ 0.22; p ¼ 0.025), DBP (r ¼ 0.27; p ¼ 0.005), waist circumference (r ¼ 0.29; p ¼ 0.002), and fat mass (r ¼ 0.24; p ¼ 0.01), and negatively with kcal/kg of body weight (r ¼ 0.22; p ¼ 0.022) – an indirect marker of physical activity (Figure 1) (Melzer et al., 2005). Multiple linear regression analysis demonstrated that in this population waist circumference and DBP were the only variables independently associated with IMT (Table 4).
Discussion Measurement of carotid IMT has gained acceptance in older adults as a non-invasive, inexpensive method to assess extent and severity of preclinical atherosclerosis. Several pieces of evidence support the validity of this measurement (Fernandes et al., 2006; Graner et al., 2006). Carotid IMT evaluated with ultrasonography correlates well with arteriosclerosis present in other arterial districts, namely in coronary vessels (Tsivgoulis et al., 2006; Van der Meer et al., 2004). Increased carotid IMT is significantly related to known cardiovascular risk factors and to the presence of carotid plaques a more advanced type of atherosclerotic lesion. Finally, carotid IMT is not only associated with stroke, coronary artery disease and peripheral vascular disease but also a reliable predictor of incident cardiovascular disease events (Oren et al., 2003; Peppa-Patrikiou et al., 1998). So far, there are limited data concerning carotid IMT in young and middle-aged adults (Burke et al., 1995; Vos et al., 2003). Our study shows that abdominal waist and DBP are the strongest predictors of higher carotid IMT in young adult males, since no other risk factors remained significantly associated with IMT after performing multivariate analysis. At first sight, it may be surprising that plasma cholesterol levels and smoking habits were not associated with IMT in our study. However, it should be underlined that our study population was selected based on perfectly normal plasma glucose, cholesterol, and triglyceride levels. Moreover, there is clear evidence that the metabolic syndrome increases the risk of cardiovascular alterations already at an early age (Takami et al., 2001; Tzou et al., 2005). However, none of the young men who participated in our study presented anthropometric and/or metabolic parameters that meet the diagnostic criteria for the metabolic syndrome according to the ATP III and AHA criteria set in 2005. Previous studies report that IMT is positively related to the prevalence of smokers and to the number of cigarettes smoked per day (Baldassarre et al., 2009). This finding was not confirmed in our study likely due to the young age of our participants. In fact, the literature is concordant in showing that the ill effects of smoking on the arterial wall are very seldom seen in very young subjects while they become evident at a later stage (Stamler et al., 2000).
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Figure 1. Spearman’s correlation analysis of measured values of intima–media thickness of the carotid bifurcation and other relevant parameters. SBP: r ¼ 0.218, p50.025 (a); DBP: r ¼ 0.27, p ¼ 0.005 (b); kcal/kg body weight: r ¼ 0.22, p ¼ 0.022 (c); waist circumference: r ¼ 0.29, p ¼ 0.0022 (d); fat mass: r ¼ 0.24, p ¼ 0.01 (e).
Table 4. Multiple linear regression independently associated with IMT. B
SE
analysis
p
of
T
the
f
variables
p
Waist circumference (cm) 0.002 0.001 0.012 2.554 7.60 50.001 DBP (mmHg) 0.002 0.001 0.034 2.146 Variables entered in the model: waist circumference, diastolic blood pressure, systolic blood pressure, BMI, fat mass and number of cigarettes smoked.
Case–control studies of children and young adults demonstrate that familial hypercholesterolemia and borderline hypertension are associated with grater IMT (Takami et al., 2001; Zhang et al., 2013). Young adults with diabetes also present with higher carotid IMT than controls (Jarvisalo et al., 2002). However, to our knowledge, this is the first study demonstrating an association between higher IMT and visceral adiposity, independently of major cardiovascular risk factors in healthy young men. This information emphasizes the need to start all lifestyle measures able to reduce/prevent abdominal obesity as early as possible. As a matter of fact already in the second decade of life, the presence of this condition is associated with preclinical markers of atherosclerosis which may later on result in clinical events. The main limitation of this study is its observational design, based on a cross-sectional evaluation. Therefore, we can only detect associations between study variables, whereas
we are unable to infer any causality. Indeed, the results of this study need to be reproduced in longitudinal studies and, possibly, in intervention trials. Other limitations are the relatively small sample size and the restriction of the observation to the male gender, which does not allow us to extrapolate our results to the female population. The main strength of our study is the evaluation of IMT and associated risk markers in a young healthy population. This is relevant to establish whether the same cardiovascular risk factors are operative in young adults as in older ones, and to decide targets for an early prevention of cardiovascular diseases in adolescents and young adults.
Conclusions In conclusion, this study shows that in a non-selected sample of healthy young adult males, a larger waist circumference and a higher diastolic blood pressure – albeit within normal values – are associated with increased carotid intima–media thickness. The results of this study highlight the potential usefulness of the IMT measurement in clinical practice also in people aged less than 30 years in order to identify people at increased cardiovascular risk. Moreover, they emphasize the need to start lifestyle interventions to prevent cardiovascular diseases already in adolescents and young adults.
Acknowledgements The authors thank Mrs. Rosanna Scala for the language editing; Mrs. Anna Maria Palumbo for the statistical analysis.
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Declaration of interest The authors report that they have no conflicts of interest.
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References Baldassarre D, Castelnuovo S, Frigerio B, Amato M, Werba JP, De Jong A, Ravani AL, et al. 2009. Effects of timing and extent of smoking, type of cigarettes, and concomitant risk factors on the association between smoking and subclinical atherosclerosis. Stroke 40:1991–1998. Burke GL, Evans GW, Riley WA, Sharrett AR, Howard G, Barnes RW, Rosamond W, et al. 1995. Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) study. Stroke 26: 386–391. Burke V. 2006. Obesity in childhood and cardiovascular risk. Clin Exp Pharmacol Physiol 33:831–837. Chambless LE, Heiss G, Folsom AR, Rosamond W, Szklo M, Sharrett AR, Clegg LX. 1997. 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 146:483–494. Davis Patricia H, Dawson Jeffrey D, Riley Ward A, Lauer Ronald M. 2001. Carotid intimal-medial thickness is related to cardiovascular risk factors measured from childhood through middle age: the Muscatine study. Circulation 104:2815–2819. Fernandes VR, Polak JF, Evdardsen T, Carvalho B, Gomes A, Bluemke DA, Nasir K, et al. 2006. Subclinical atherosclerosis and incipient regional myocardial dysfunction in asymptomatic individuals: the Multi-Ethnic Study of Atherosclerosis (MESA). J Am Coll Cardiol 47:2420–2428. Graner M, Varpula M, Kahri J, Salonen RM, Nyysso¨nen K, Nieminen MS, Taskinen MR, Syva¨nne M. 2006. Association of carotid intima– media thickness with angiographic severity and extent of coronary artery disease. Am J Cardiol 97:624–629. Heiss G, Sharrett AR, Barnes R, Chambless LE, Szklo M, Alzola C. 1991. Carotid atherosclerosis measured by B-mode ultrasound in populations: associations with cardiovascular risk factors in ARIC study. Am J Epidemiol 134:250–256. Herouvi D, Karanasios E, Karayianni C, Karavanaki K. 2013. Cardiovascular disease in childhood: the role of obesity. Eur J Pediatr 172:721–732. Jarvisalo MJ, Putto-Laurila A, Jartti L, Lehtima¨ki T, Solakivi T, Ro¨nnemaa T, Raitakari OT. 2002. Carotid artery intima–media thickness in children with type 1 diabetes. Diabetes 51:493–498. Johnson HM, Douglas PS, Srinivasan SR, Bond MG, Tang R, Li S, Chen W, et al. 2007. Predictors of carotid intima–media thickness progression in young adults: the Bogalusa Heart Study. Stroke 38: 900–905. Lorenz MW, Polak JF, Kavousi M, Mathiesen EB, Vo¨lzke H, Tuomainen TP, Sander D, et al., PROG-IMT Study Group. 2012. Carotid intima–media thickness progression to predict cardiovascular events in the general population (the PROG-IMT collaborative project): a meta-analysis of individual participant data. Lancet 379: 2053–2062. Lukaski HC, Bolonchuk WW, Hall CB, Siders WA. 1986. Validation of tetrapolar bioelectrical impedence method to assess human body composition. J Appl Physiol 60:1327–1332. McGill Jr HC, McMahan CA, Herderick EE, Tracy RE, Malcom GT, Zieske AW, Strong JP for the PDAY Research Group. 2000. Effects of coronary research disease risk factors on atherosclerosis of selected regions of aorta and right coronary artery. Arterioscler Thromb Vasc Biol 20:836–845.
Int J Food Sci Nutr, 2015; 66(4): 466–470
Melzer K, Kayser B, Saris WH, Pichard C. 2005. Effects of physical activity on food intake. Clin Nutr 24:885–895. Oren A, Vos LE, Uiterwaal CS, Grobbee DE, Bots ML. 2003. Cardiovascular risk factors and increased carotid intima–media thickness in healthy young adults: the ARYA Study. Arch Intern Med 163: 1787–1792. PDAY Research Group. 1990. Relationship of atherosclerosis in young men to serum lipoprotein cholesterol concentrations and smoking: a preliminary report from the. JAMA 264:3018–3024. Peppa-Patrikiou M, Scordili M, Antoniu A, Giannaki M, Dracopoulou M, Dacou-Voutetakis C. 1998. Carotid atherosclerosis in adolescents and young adults with IDDM. Diabetes Care 21:1004–1007. Pignoli P. 1984. Ultrasound B-mode imaging for arterial wall thickness measurement. Atheroscler Rev 12:177–184. Raikatari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Ma¨kiTorkko N, Ja¨rvisalo MJ, et al. 2003. Cardiovascular risk factors in childhood and carotid artery intima–media thickness in adulthood. JAMA 290:2277–2283. Riley WA, Barnes RW, Applegate WB, Dempsey R, Hartwell T, Davis VG, Bond MG, Furberg CD. 1992. Reproducibility of non-invasive ultrasonic measurement of carotid atherosclerosis: the Asymptomatic Carotid Artery Plaque Study. Stroke 23: 1062–1068. Salonen JT, Salonen R. 1991. Ultrasonographically assessed carotid morphology and the risk of coronary heart disease. Arterioscler Thromb 11:1245–1249. Short KR, Blackett PR, Gardner AW, Copeland KC. 2009. Vascular health in children and adolescents: effects of obesity and diabetes. Vasc Health Risk Manag 5:973–990. Simon A, Megnien JL, Chironi G. 2010. The value of carotid intima– media thickness for predicting cardiovascular risk. Arterioscler Thromb Vasc Biol 30:182–185. Stamler J, Daviglus ML, Garside DB, Greenland P, Neaton JD. 2000. Relation of baseline serum cholesterol levels in 3 large cohorts of younger men to long-term coronary, cardiovascular, and all cause mortality and to longevity. JAMA 284:311–318. Takami R, Takeda N, Hayashi M, Sasaki A, Kawachi S, Yoshino K, Takami K, et al. 2001. Body fatness and fat distribution as predictors of metabolic abnormalities and early carotid atherosclerosis. Diabetes Care 24:1248–1252. Trevisan M, Krogh V, Ferro-Luzzi A, Riccardi G, Freudenheim J, Sette S, Scaccini C. 1992. Food questionnaire for epidemiological studies on large cohorts for use in Italy. Ann Ist Supe Sanita` 28:397–401. Tsivgoulis G, Vemmos K, Papamichael C, Spengos K, Manios E, Stamatelopoulos K, Vassilopoulos D, Zakopoulos N. 2006. Common carotid artery intima–media thickness and the risk of stroke recurrence. Stroke 37:1913–1916. Tzou WS, Douglas PS, Srinivasan SR, Bond MG, Tang R, Chen W, et al. 2005. Increased subclinical atherosclerosis in young adults with metabolic syndrome. J Am Coll Cardiol 46:457–463. Van der Meer IM, Bots ML, Hofman A, del Sol AI, van der Kuip DA, Witteman JC. 2004. Predictive value of noninvasive measures of atherosclerosis for incident myocardial infarction: the Rotterdam Study. Circulation 109:1089–1094. Vos LE, Oren A, Uiterwaal CS, Gorissen WH, Grobbee DE, Bots ML. 2003. Adolescent blood pressure and blood pressure tracking into young adulthood are related to subclinical atherosclerosis: the Atherosclerosis Risk in Young Adults (ARYA) study. Am J Hypertension 16:549–555. Zhang ZQ, Deng J, He LP, Ling WH, Su YX, Chen YM. 2013. Comparison of various anthropometric and body fat indices in identifying cardiometabolic disturbances in Chinese men and women. PLoS One 8:e70893.
