Skip to main content
Log in

Metabolic syndrome showed significant relationship with carotid atherosclerosis

  • Original Article
  • Published:
Heart and Vessels Aims and scope Submit manuscript

Abstract

Metabolic syndrome (MetS) is associated with an increased risk of cardiovascular disease. We assessed the associations between MetS and the indicators of carotid atherosclerosis as assessed by ultrasonography taking into consideration of confounders in the general population. A total of 1281 subjects (856 males, 425 females) were included in the present study. The total plaque score and maximum intima-media thickness (IMT) of the carotid arteries were measured as indicators of atherosclerosis. Cardiovascular risk factors were several metabolic components, serum uric acid, serum C-reactive protein (CRP), and lifestyle factors. MetS was defined according to the criteria of the National Cholesterol Education Program. The prevalences of an elevated total plaque score (≥5) and elevated IMT (>1 mm) of the carotid arteries were significantly higher in subjects with MetS as compared to subjects without MetS. Furthermore, a trend was observed towards higher prevalences of these indicators of atherosclerosis as the number of components of MetS increased. Logistic regression analysis revealed a significant association between elevated plaque score and MetS even after adjustments for age, serum uric acid, serum CRP and lifestyle factors in the males. Among the indicators of atherosclerosis assessed by carotid ultrasonography, a significant independent association was observed between the total plaque score and MetS in males in the general population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Dekker JM, Girman C, Rhodes T, Nijpels G, Stehouwer CD, Bouter LM, Heine RJ (2005) Metabolic syndrome and 10-year cardiovascular disease risk in the Hoorn Study. Circulation 112:666–673

    Article  PubMed  Google Scholar 

  2. Mottillo S, Filion KB, Genest J, Joseph L, Pilote L, Poirier P, Rinfret S, Schiffrin EL, Eisenberg MJ (2010) The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol 56:1113–1132

    Article  PubMed  Google Scholar 

  3. Ford ES (2005) Risks for all-cause mortality, cardiovascular disease, and diabetes associated with the metabolic syndrome: a summary of the evidence. Diabetes Care 28:1769–1778

    Article  PubMed  Google Scholar 

  4. Ma X, Zhu S (2013) Metabolic syndrome in the prevention of cardiovascular diseases and diabetes—still a matter of debate? Eur J Clin Nutr 67:518–521

    Article  CAS  PubMed  Google Scholar 

  5. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 285:2486–2497

    Article  Google Scholar 

  6. Unwin N, Bhopal R, Hayes L, White M, Patel S, Ragoobirsingh D, Alberti G (2007) A comparison of the new international diabetes federation definition of metabolic syndrome to WHO and NCEP definitions in Chinese, European and South Asian origin adults. Ethn Dis 17:522–528

    PubMed  Google Scholar 

  7. Delavari A, Forouzanfar MH, Alikhani S, Sharifian A, Kelishadi R (2009) First nationwide study of the prevalence of the metabolic syndrome and optimal cutoff points of waist circumference in the Middle East: the national survey of risk factors for noncommunicable diseases of Iran. Diabetes Care 32:1092–1097

    Article  PubMed  PubMed Central  Google Scholar 

  8. Sipilä K, Moilanen L, Nieminen T, Reunanen A, Jula A, Salomaa V, Kaaja R, Kukkonen-Harjula K, Lehtimäki T, Kesäniemi YA, Koivistoinen T, Nieminen MS, Tuomilehto J, Kähönen M (2009) Metabolic syndrome and carotid intima media thickness in the health 2000 survey. Atherosclerosis 204:276–281

    Article  PubMed  Google Scholar 

  9. Nguyen-Thanh HT, Benzaquen BS (2009) Screening for subclinical coronary artery disease measuring carotid intima media thickness. Am J Cardiol 104:1383–1388

    Article  PubMed  Google Scholar 

  10. Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M (2007) Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 115:459–467

    Article  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. Inaba Y, Chen JA, Bergmann SR (2012) Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis 220:128–133

    Article  CAS  PubMed  Google Scholar 

  13. Plichart M, Celermajer DS, Zureik M, Helmer C, Jouven X, Ritchie K, Tzourio C, Ducimetière P, Empana JP (2011) Carotid intima-media thickness in plaque-free site, carotid plaques and coronary heart disease risk prediction in older adults. The Three-City Study. Atherosclerosis 219:917–924

    Article  CAS  PubMed  Google Scholar 

  14. van den Oord SC, Sijbrands EJ, ten Kate GL, van Klaveren D, van Domburg RT, van der Steen AF, Schinkel AF (2013) Carotid intima-media thickness for cardiovascular risk assessment: systematic review and meta-analysis. Atherosclerosis 228:1–11

    Article  PubMed  Google Scholar 

  15. Den Ruijter HM, Peters SA, Anderson TJ, Britton AR, Dekker JM, Eijkemans MJ, Engström G, Evans GW, de Graaf J, Grobbee DE, Hedblad B, Hofman A, Holewijn S, Ikeda A, Kavousi M, Kitagawa K, Kitamura A, Koffijberg H, Lonn EM, Lorenz MW, Mathiesen EB, Nijpels G, Okazaki S, O’Leary DH, Polak JF, Price JF, Robertson C, Rembold CM, Rosvall M, Rundek T, Salonen JT, Sitzer M, Stehouwer CD, Witteman JC, Moons KG, Bots ML (2012) Common carotid intima-media thickness measurements in cardiovascular risk prediction: a meta-analysis. JAMA 308:796–803

    Article  Google Scholar 

  16. Lorenz MW, Polak JF, Kavousi M, Mathiesen EB, Völzke H, Tuomainen TP, Sander D, Plichart M, Catapano AL, Robertson CM, Kiechl S, Rundek T, Desvarieux M, Lind L, Schmid C, DasMahapatra P, Gao L, Ziegelbauer K, Bots ML, Thompson SG, 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

    Article  PubMed  PubMed Central  Google Scholar 

  17. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr, International Diabetes Federation Task Force on Epidemiology and Prevention, National Heart, Lung, and Blood Institute, American Heart Association; World Heart Federation, International Atherosclerosis Society, International Association for the Study of Obesity (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on epidemiology and prevention; national heart, lung, and blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120:1640–1645

    Article  CAS  PubMed  Google Scholar 

  18. del Sol AI, Moons KG, Hollander M, Hofman A, Koudstaal PJ, Grobbee DE, Breteler MM, Witteman JC, Bots ML (2001) Is carotid intima-media thickness useful in cardiovascular disease risk assessment? The Rotterdam Study. Stroke 32:1532–1538

    Article  PubMed  Google Scholar 

  19. O’Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr (1999) Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med 340:14–22

    Article  PubMed  Google Scholar 

  20. Bots ML, Hoes AW, Koudstaal PJ, Hofman A, Grobbee DE (1997) Common carotid intima-media thickness and risk of stroke and myocardial infarction: the Rotterdam Study. Circulation 96:1432–1437

    Article  CAS  PubMed  Google Scholar 

  21. Spence JD (2006) Measurement of intima-media thickness versus carotid plaque: uses in patient care, genetic research and evaluation of new therapies. Int J Stroke 1:216–221

    Article  PubMed  Google Scholar 

  22. Johnsen SH, Mathiesen EB (2009) Carotid plaque compared with intima-media thickness as a predictor of coronary and cerebrovascular disease. Curr Cardiol Rep 11:21–27

    Article  PubMed  Google Scholar 

  23. Pollex RL, Al-Shali KZ, House AA, Spence JD, Fenster A, Mamakeesick M, Zinman B, Harris SB, Hanley AJ, Hegele RA (2006) Relationship of the metabolic syndrome to carotid ultrasound traits. Cardiovasc Ultrasound 4:28

    Article  PubMed  PubMed Central  Google Scholar 

  24. Chen PC, Chien KL, Hsu HC, Su TC, Chang CW, Sung FC, Lee YT (2008) C-reactive protein and the metabolic syndrome correlate differently with carotid atherosclerosis between men and women in a Taiwanese community. Metabolism 57:1023–1028

    Article  CAS  PubMed  Google Scholar 

  25. Kalish GM, Barrett-Connor E, Laughlin GA, Gulanski BI (2003) Postmenopausal estrogen/progestin intervention trial. Association of endogenous sex hormones and insulin resistance among postmenopausal women: results from the postmenopausal estrogen/progestin intervention trial. J Clin Endocrinol Metab 88:1646–1652

    Article  CAS  PubMed  Google Scholar 

  26. Jiang CQ, Xu L, Lam TH, Lin JM, Cheng KK, Thomas GN (2010) Smoking cessation and carotid atherosclerosis: the Guangzhou Biobank Cohort Study–CVD. J Epidemiol Community Health 64:1004–1009

    Article  CAS  PubMed  Google Scholar 

  27. Amarenco P, Labreuche J, Touboul PJ (2008) High-density lipoprotein-cholesterol and risk of stroke and carotid atherosclerosis: a systematic review. Atherosclerosis 196:489–496

    Article  CAS  PubMed  Google Scholar 

  28. Madjid M, Willerson JT (2011) Inflammatory markers in coronary heart disease. Br Med Bull 100:23–38

    Article  CAS  PubMed  Google Scholar 

  29. Koenig W (2005) Predicting risk and treatment benefit in atherosclerosis: the role of C-reactive protein. Int J Cardiol 98:199–206

    Article  PubMed  Google Scholar 

  30. Kampus P, Kals J, Ristimäe T, Muda P, Ulst K, Zilmer K, Salonen RM, Tuomainen TP, Teesalu R, Zilmer M (2007) Augmentation index and carotid intima-media thickness are differently related to age, C-reactive protein and oxidized low-density lipoprotein. J Hypertens 25:819–825

    Article  CAS  PubMed  Google Scholar 

  31. Thakore AH, Guo CY, Larson MG, Corey D, Wang TJ, Vasan RS, D’Agostino RB Sr, Lipinska I, Keaney JF Jr, Benjamin EJ, O’Donnell CJ (2007) Association of multiple inflammatory markers with carotid intimal medial thickness and stenosis (from the Framingham Heart Study). Am J Cardiol 99:1598–1602

    Article  PubMed  Google Scholar 

  32. Ahluwalia N, Drouet L, Ruidavets JB, Perret B, Amar J, Boccalon H, Hanaire-Broutin H, Ferrières J (2006) Metabolic syndrome is associated with markers of subclinical atherosclerosis in a French population-based sample. Atherosclerosis 186:345–353

    Article  CAS  PubMed  Google Scholar 

  33. Ridker PM, Buring JE, Cook NR, Rifai N (2003) C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14719 initially healthy American women. Circulation 107:391–397

    Article  PubMed  Google Scholar 

  34. Bisoendial RJ, Boekholdt SM, Vergeer M, Stroes ES, Kastelein JJ (2010) C-reactive protein is a mediator of cardiovascular disease. Eur Heart J 31:2087–2091

    Article  CAS  PubMed  Google Scholar 

  35. Yousuf O, Mohanty BD, Martin SS, Joshi PH, Blaha MJ, Nasir K, Blumenthal RS, Budoff MJ (2013) High-sensitivity C-reactive protein and cardiovascular disease: a resolute belief or an elusive link? J Am Coll Cardiol 62:397–408

    Article  CAS  PubMed  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. Prati P, Tosetto A, Casaroli M, Bignamini A, Canciani L, Bornstein N, Prati G, Touboul PJ (2011) Carotid plaque morphology improves stroke risk prediction: usefulness of a new ultrasonographic score. Cerebrovasc Dis 31:300–304

    Article  CAS  PubMed  Google Scholar 

  38. Rundek T, Arif H, Boden-Albala B, Elkind MS, Paik MC, Sacco RL (2008) Carotid plaque, a subclinical precursor of vascular events: the Northern Manhattan Study. Neurology 70:1200–1207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Oda E (2014) Serum uric acid is an independent predictor of metabolic syndrome in a Japanese health screening population. Heart Vessels 29:496–503

    Article  PubMed  Google Scholar 

  40. Okumura K, Tsukamoto H, Tsuboi H, Hirayama H, Kamiya H, Watarai M, Ishiki R, Murohara T (2014) High HDL cholesterol level after treatment with pitavastatin is an important factor for regression in carotid intima-media thickness. Heart Vessels. doi:10.1007/s00380-013-0466-3

    Google Scholar 

  41. Rossi A, Faggiano P, Amado AE, Cicoira M, Bonapace S, Franceschini L, Dini FL, Ghio S, Agricola E, Temporelli PL, Vassanelli C (2014) Mitral and aortic valve sclerosis/calcification and carotid atherosclerosis: results from 1065 patients. Heart Vessels 29:776–783

    Article  PubMed  Google Scholar 

  42. Tani S, Nagao K, Hirayama A (2015) Association of atherosclerosis-related markers and its relationship to n-3 polyunsaturated fatty acids levels with a prevalence of coronary artery disease in an urban area in Japan. Heart Vessels 30:9–19

    Article  PubMed  Google Scholar 

  43. Henry RM, Kostense PJ, Dekker JM, Nijpels G, Heine RJ, Kamp O, Bouter LM, Stehouwer CD (2004) Carotid arterial remodeling: a maladaptive phenomenon in type 2 diabetes but not in impaired glucose metabolism: the Hoorn study. Stroke 35:671–676

    Article  PubMed  Google Scholar 

  44. Temelkova-Kurktschiev TS, Koehler C, Leonhardt W, Schaper F, Henkel E, Siegert G, Hanefeld M (1999) Increased intimal-medial thickness in newly detected type 2 diabetes: risk factors. Diabetes Care 22:333–338

    Article  CAS  PubMed  Google Scholar 

  45. Kato K, Otsuka T, Kobayashi N, Kon Y, Kawada T (2014) Two-hour post-load plasma glucose levels are associated with carotid intima-media thickness in subjects with normal glucose tolerance. Diabet Med 31:76–83

    Article  CAS  PubMed  Google Scholar 

  46. Ballantyne CM, Hoogeveen RC, McNeill AM, Heiss G, Schmidt MI, Duncan BB, Pankow JS (2008) Metabolic syndrome risk for cardiovascular disease and diabetes in the ARIC study. Int J Obes 32(Suppl 2):S21–S24

    Article  CAS  Google Scholar 

  47. Kawamoto R, Tomita H, Ohtsuka N, Inoue A, Kamitani A (2007) Metabolic syndrome, diabetes and subclinical atherosclerosis as assessed by carotid intima-media thickness. J Arteroscler Thromb 14:78–85

    Article  CAS  Google Scholar 

  48. Zanchetti A, Hennig M, Baurecht H, Tang R, Cuspidi C, Carugo S, Mancia G (2007) Prevalence and incidence of the metabolic syndrome in the European Lacidipine Study on atherosclerosis (ELSA) and its relation with carotid intima-media thickness. J Hypertens 25:2463–2470

    Article  CAS  PubMed  Google Scholar 

  49. Herder M, Arntzen KA, Johnsen SH, Mathiesen EB (2012) The metabolic syndrome and progression of carotid atherosclerosis over 13 years. The Tromsø Study. Cardiovasc Diabetol 11:77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Rundek T, White H, Boden-Albala B, Jin Z, Elkind MS, Sacco RL (2007) The metabolic syndrome and subclinical carotid atherosclerosis: the Northern Manhattan Study. J Cardiometabol Syndr 2:24–29

    Article  Google Scholar 

  51. Della-Morte D, Gardener H, Denaro F, Boden-Albala B, Elkind MS, Paik MC, Sacco RL, Rundek T (2010) Metabolic syndrome increases carotid artery stiffness: the Northern Manhattan Study. Int J Stroke 5:138–144

    Article  PubMed  PubMed Central  Google Scholar 

  52. Bonora E, Kiechl S, Willeit J, Oberhollenzer F, Egger G, Bonadonna RC, Muggeo M, Bruneck study (2003) Carotid atherosclerosis and coronary heart disease in the metabolic syndrome: prospective data from the Bruneck study. Diabetes Care 26:1251–1257

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to express our appreciation to the study participants. This work was supported partly by Grant-in-Aid for Scientific Research (C) (24590763), which was given by the Japan Society for the Promotion of Science.

Conflict of interest

The authors declare that they have no conflict of interest in this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomoyuki Kawada.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kawada, T., Andou, T. & Fukumitsu, M. Metabolic syndrome showed significant relationship with carotid atherosclerosis. Heart Vessels 31, 664–670 (2016). https://doi.org/10.1007/s00380-015-0668-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00380-015-0668-y

Keywords

Navigation