Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Epidemiological evidence for the non-random clustering of the components of the metabolic syndrome: multicentre study of the Mediterranean Group for the Study of Diabetes

European Journal of Clinical Nutrition volume 60, pages 1376–1383 (2006)Cite this article

Abstract

Objective:

To determine: (a) whether the components of metabolic syndrome (MetS) cluster more frequently than predicted by chance alone and (b) whether increased risk for MetS is associated also with values of each component below, but close to the cutoff points defining MetS.

Research design and methods:

Anthropometrical and biochemical measurements were performed and a dietary questionnaire was filled-in in 1833 randomly selected non-diabetic subjects, 916 men and 917 women, 20–74 years old, in nine centres in five Mediterranean countries. The prevalence of MetS and of possible combinations of its individual components was measured. The expected frequencies of the above combinations were calculated according to the mathematical formula of probabilities.

Results:

The overall prevalence of MetS was 27.2%, but varied greatly among countries, from 5.8% in Algeria to 37.3% in Greece. The observed prevalence of each combination diagnostic of MetS was higher than the expected by chance. Thus, the observed overall prevalence of MetS was also higher than the expected, 27.2 vs 24.0%, P=0.03. Furthermore, for each individual component (except high-density lipoprotein), as values in the normal range, approached the cutoff point, the risk of having MetS (i.e. clustering of the other components) increased significantly (odds ratio 2.2–4.6, P<0.001).

Conclusions:

The MetS is not related to the Mediterranean type of diet and its prevalence varies greatly among five Mediterranean countries. The clustering of the components defining the MetS is not due to chance and moreover even ‘high normal’ levels of each component confer increased risk for the syndrome.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  • Alexander CM, Landsman PB, Teutsch SM, Haffner SM, Third National Health and Nutrition Examination Survey (NHANES III); National Cholesterol Education Program (NCEP) (2003). NCEP-defined metabolic syndrome, diabetes, and prevalence of coronary heart disease among NHANES III participants age 50 years and older. Diabetes 52, 1210–1214.

    Article  CAS  PubMed  Google Scholar 

  • American Diabetes Association (2005). Diagnosis and classification of diabetes mellitus. Diabetes Care 28 (Suppl 1), S5–S10.

  • Armitage P (1983). The meaning of probability. In: Statistical Methods in Medical Research. Blackwell Scientific Publications: Oxford. ISBN 0 632 05430 1. pp. 44.–52.

    Google Scholar 

  • Athyros VG, Ganotakis ES, Elisaf M, Mikhailidis DP (2005). The prevalence of the metabolic syndrome using the National Cholesterol Educational Program and International Diabetes Federation definitions. Curr Med Res Opin 21, 1157–1159.

    Article  PubMed  Google Scholar 

  • Cameron A, Shaw J, Zimmet P (2004). The metabolic syndrome: prevalence in worldwide populations. Endocrinol Metab Clin North Am 33, 351–375.

    Article  PubMed  Google Scholar 

  • Carnethon MR, Loria CM, Hill JO, Sidney S, Savage PJ, Liu K, Coronary Artery Risk Development in Young Adults Study (2004). Risk factors for the metabolic syndrome: the Coronary Artery Risk Development in Young Adults (CARDIA) study, 1985–2001. Diabetes Care 27, 2707–2715.

    Article  PubMed  Google Scholar 

  • Eckel R, Grundy S, Zimmet P (2005). The metabolic syndrome. Lancet 365, 1415–1428.

    Article  CAS  PubMed  Google Scholar 

  • Ford ES, Giles WH, Mokdad AH (2004). Increasing prevalence of the metabolic syndrome among US adults. Diabetes Care 27, 2444–2449.

    Article  PubMed  Google Scholar 

  • Ford ES, Giles WH, Dietz WH (2002). Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 287, 356–359.

    Article  PubMed  Google Scholar 

  • Girman CJ, Rhodes T, Mercuri M, Pyorala K, Kjekshus J, Pedersen TR et al. (2004). The metabolic syndrome and risk of major coronary events in the Scandinavian simvastatin survival study (4S) and the air force/texas coronary atherosclerosis prevention study (AFCAPS/TexCAPS). Am J Cardiol 93, 136–141.

    Article  CAS  PubMed  Google Scholar 

  • Golden S, Folsom A, Coresh J, Sharrett R, Szklo M, Brancati F (2002). Risk factor groupings related to insulin resistance and their synergistic effects on subclinical atherosclerosis. The atherosclerosis risk in communities' study. Diabetes 51, 3069–3076.

    Article  CAS  PubMed  Google Scholar 

  • Groop L (2000). Genetics of the metabolic syndrome. Br J Nutr 83 (Suppl 1), S39–S48.

    CAS  PubMed  Google Scholar 

  • Grundy SM, Brewer Jr HB, Cleeman Jr JI, Smith SC, Lenfant C, American Heart Association; National Heart, Lung, and Blood Institute (2004). Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 109, 433–438.

    Article  PubMed  Google Scholar 

  • Grundy SM (2004). What is the contribution of obesity to the metabolic syndrome? Endocrinol Metab Clin North Am 33, 267–282.

    Article  PubMed  Google Scholar 

  • Haffner SM, D' Agostino Jr R, Mykkanen L, Tracy R, Howard B, Rewers M et al. (1999). Insulin sensitivity in subjects with type 2 diabetes: relationship to cardiovascular risk factors. The insulin resistance atherosclerosis study. Diabetes Care 22, 562–568.

    Article  CAS  PubMed  Google Scholar 

  • Haffner SM, Valdez RA, Hazuda HP, Mitchell BD, Morales PA, Stern MP (1992). Prospective analysis of the insulin resistance syndrome (Syndrome X). Diabetes 41, 715–722.

    Article  CAS  PubMed  Google Scholar 

  • Haffner SM, D' Agostino R, Saad MF, Rewers M, Mykkanen L, Selby J et al. (1996). Increased insulin resistance and insulin secretion in nondiabetic African-Americans and Hispanics compared with non-Hispanic whites. The Insulin Resistance Atherosclerosis Study. Diabetes 45, 742–748.

    Article  CAS  PubMed  Google Scholar 

  • Isomaa B, Almgren P, Tuomi T, Forsen B, Lahti K, Nissen M et al. (2001). Cardiovascular morbidity and mortality associated with the Metabolic Syndrome. Diabetes Care 24, 683–689.

    Article  CAS  PubMed  Google Scholar 

  • Karamanos B (1996). Interim report of the nutrition study group of the Mediterranean group for the study of diabetes (MGSD). Medicographia 18 (Suppl 1), 38–40.

    Google Scholar 

  • Karamanos B, Thanopoulou A, Angelico F, Assaad-Khalil S, Barbato A, Del ben M et al. (2002). Nutritional habits in the Mediterranean basin. The macronutrient composition of diet and its relation with the traditional Mediterranean diet. Multi-Center Study of the Mediterranean Group for the Study of Diabetes (MGSD). Eur J Clin Nutr 56, 983–991.

    Article  CAS  PubMed  Google Scholar 

  • Klein B, Klein R, Lee K (2002). Components of the metabolic syndrome and risk of cardiovascular disease and diabetes in Beaver Dam. Diabetes Care 25, 1790–1794.

    Article  PubMed  Google Scholar 

  • Kromhout D, Keys A, Aravanis C, Buzina R, Fidanza F, Giampaoli S (1989). Food consumption patterns in the 1960s in seven countries. Am J Clin Nutr 49, 889–894.

    Article  CAS  PubMed  Google Scholar 

  • Kylin E (1923). Studies of the hypertension – hyperglycemia – hyperuricemia syndrome (Studien ueber das hypertonie – hyperglykamie – hyperurikamie syndrome). Zentralblatt fuer Innere Medizin 44, 105–127.

    Google Scholar 

  • Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomileto J et al. (2002). Themetabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA 288, 2709–2716.

    Article  PubMed  Google Scholar 

  • Lee YJ, Tsai J (2002). ACE gene insertion/deletion polymorphism associated with 1998 world health organization definition of metabolic syndrome in Chinese type 2 diabetic patients. Diabetes Care 25, 1002–1008.

    Article  CAS  PubMed  Google Scholar 

  • Malik S, Wong N, Franklin S, Kamath T, L'Italien G, Pio J et al. (2004). Impact of the metabolic syndrome on mortality from coronary heart disease, cardiovascular disease, and all causes in United States adults. Circulation 110, 1245–1250.

    Article  PubMed  Google Scholar 

  • McNeill AM, Rosamond WD, Girman CJ, Golden SH, Schmidt MI, East HE et al. (2005). The metabolic syndrome and 11-year risk of incident cardiovascular disease in the Atherosclerosis Risk In Communities study. Diabetes Care 28, 385–390.

    Article  PubMed  Google Scholar 

  • Meigs JB, D' Agostino Sr RB, Wilson PW, Cupples LA, Nathan DM, Singer DE (1997). Risk variable clustering in the insulin resistance syndrome. The Framingham Offspring Study. Diabetes 46, 1594–1600.

    Article  CAS  PubMed  Google Scholar 

  • Mykkanen L, Kuusisto J, Pyorala K, Laakso M (1993). Cardiovascular disease risk factors as predictors of type 2 (non-insulin-dependent) diabetes mellitus in elderly subjects. Diabetologia 36, 553–559.

    Article  CAS  PubMed  Google Scholar 

  • National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) (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.

  • Olijhoek J, van der Graaf Y, Banga JD, Algra A, Rabelink T, Visseren F (2004). The metabolic syndrome is associated with advanced vascular damage in patients with coronary heart disease, stroke, peripheral arterial disease or abdominal aortic aneurism. Eur Heart J 25, 342–348.

    Article  PubMed  Google Scholar 

  • Palaniappan L, Carnethon M, Wang Y, Hanley A, Fortmann S, Haffner S et al. (2004). Predictors of the incident Metabolic Syndrome in adults. Diabetes Care 27, 788–793.

    Article  PubMed  Google Scholar 

  • Reaven GM (1988). Banting Lecture 1988: Role of insulin resistance in human disease. Diabetes 37, 1595–1607.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt MI, Watson RL, Duncan BB, Metcalf P, Brancati FL, Sharrett AR et al. (1996). Clustering of dyslipidemia, hyperuricemia, diabetes, and hypertension and its association with fasting insulin and central and overall obesity in a general population. Atherosclerosis Risk in Communities Study Investigators. Metabolism 45, 699–706.

    Article  CAS  PubMed  Google Scholar 

  • Stern M, Williams K, Gonzalez-Villalpando C, Hunt K, Haffner S (2004). Does the metabolic syndrome improve identification of individuals at risk of type 2 diabetes and/or cardiovascular disease? Diabetes Care 27, 2676–2681.

    Article  PubMed  Google Scholar 

  • Trichopoulou A, Costacou T, Bamia Ch, Trichopoulos D (2003). Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348, 2599–2608.

    Article  PubMed  Google Scholar 

  • Trichopoulou A, Kouris-Blazos A, Wahlqvist M, Gnardellis Ch, Lagiou P, Polychronopoulos E et al. (1995). Diet and overall survival in elderly people. BMJ 311, 1457–1460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trichopoulou A, Orphanos Ph, Norat T, Bueno-de-Mesquita B, Ocki M, Peeters P et al. (2005). Modified Mediterranean diet and survival: EPIC-elderly prospective cohort study. BMJ 330, 991–998.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson P, Kannel W, Silbershatz H, D' Agostino R (1999). Clustering of metabolic factors and coronary heart disease. Arch Intern Med 159, 1104–1109.

    Article  CAS  PubMed  Google Scholar 

  • World Data Table http://who.org/cvd_atlas_29_world_data_table.pdf.

Download references

Acknowledgements

We thank all the subjects who took part in this study. The study is part of the MultiCentre Nutritional Study of the Mediterranean Group for the Study of Diabetes (MGSD). We thank Ms E Antoniadou and Ms M Panagiotopoulou for secretarial support and Ms P Maraki for laboratory assistance.

Author information

Authors and Affiliations

  1. 2nd Department of Internal Medicine, Diabetes Centre, National University of Athens, Hippokration General Hospital, Athens, Greece

    A Thanopoulou, B Karamanos, D Roussi & A Archimandritis

  2. Department of Medical Therapy, University ‘La Sapienza’, Rome, Italy

    F Angelico

  3. Department of Internal Medicine, Alexandria Faculty of Medicine, Alexandria, Egypt

    S Assaad-Khalil

  4. Diabetes Centre, Institute for Endocrinology, Diabetes and Metabolic Diseases, Clinical Centre of Serbia, Belgrade, Serbia, Montenegro

    P Djordjevic

  5. 1st Department of Propedeutic Medicine, Diabetes Centre, Athens University School of Medicine, ‘Laiko’ General Hospital, Athens, Greece

    N Katsilambros

  6. Diabetes Centre, ‘NIMTS’ Hospital, Athens, Greece

    I Migdalis

  7. Service of Internal Medicine ‘A’ C.H.U., Oran, Algeria

    M Mrabet

  8. Diabetes Centre ‘St. Luca’,, Sofia, Bulgaria

    M Petkova

  9. Department of Preventive, Occupational and Community Medicine. Section of Hygiene, University of Studies of Pavia, Italy

    M-T Tenconi

Authors
  1. A Thanopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B Karamanos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F Angelico
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S Assaad-Khalil
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P Djordjevic
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N Katsilambros
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. I Migdalis
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M Mrabet
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M Petkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. D Roussi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. M-T Tenconi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. A Archimandritis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B Karamanos.

Additional information

Guarantors: B Karamanos.

Contributors: AT and BK conducted the statistical analysis and wrote the intial draft. All authors participated in the design, interpretation and writing up of the research work.

Participating centres

Professor B Karamanos (Co-ordinator), A Thanopoulou, D Roussi

Diabetes Centre, 2nd Medical Department, Athens University Medical School, Hippokration Hospital, Athens, Greece

Professor F Angelico, M Del Ben, A Barbato

Department of Clinics and Applied Medical Therapy, University ‘La Sapienza’, Rome, Italy

Professor S Assaad Khalil

Department of Internal Medicine, Alexandria Faculty of Medicine, Alexandria, Egypt

Professor P Djordjevic, V Dimitrijevic-Sreckovic, F Canovic

Diabetes Centre, Institute for Endocrinology, Diabetes and Metabolic Diseases, Clinical Centre of Serbia, Belgrade, Yugoslavia.

Professor N Katsilambros

Diabetes Centre, 1st Department of Propedeutic Medicine, Athens University School of Medicine, Laiko General Hospital, Athens, Greece

Dr I Migdalis

Diabetes Centre, ‘ÍÉÌÔS’ Hospital, Athens, Greece

Dr M Mrabet, S Zarat, A Bentounsi

Service de Medicine Interne ‘A’ CHU Oran, Algeria

Dr M Petkova

Diabetes Centre ‘St Luca’, Sofia, Bulgaria

Professor MT Tenconi, C Gallotti

Dipartimento di Medicina Preventiva, Occupazionale e di Communita. Sezione di Igiene. Universita degli studi di Pavia, Italy

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thanopoulou, A., Karamanos, B., Angelico, F. et al. Epidemiological evidence for the non-random clustering of the components of the metabolic syndrome: multicentre study of the Mediterranean Group for the Study of Diabetes. Eur J Clin Nutr 60, 1376–1383 (2006). https://doi.org/10.1038/sj.ejcn.1602467

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.ejcn.1602467

Keywords

This article is cited by

Search

Advanced search

Quick links