Skip to main content
Intended for healthcare professionals
Restricted access
Research article
First published online January 4, 2018

The association between metabolic syndrome and its components with systemic lupus erythematosus: a comprehensive systematic review and meta-analysis of observational studies

Abstract

Objectives

Based upon inflammatory-related factors in chronic systemic lupus erythematosus (SLE), as well as the long-term prescription of corticosteroids, metabolic syndrome (MetS) prevalence is expected to be higher in SLE patients than among those without SLE. The aim of this study was to systematically analyze: (1) the worldwide prevalence of MetS in patients with SLE using different criteria, (2) the risk of MetS in patients with SLE compared with those without SLE, and (3) the risk of MetS component in patients with SLE compared with healthy controls.

Methods

We searched international databases, such as: Web of Science, Medline, PubMed, Scopus, Embase, CABI, CINAHL, DOAJ and Google Scholar. The articles which reported the prevalence of MetS in SLE patients, between 2006 and 2017, were included in the study if they had a: clear study design, study time and location, sound sampling approach and appropriate statistical analyses. Studies without sufficient data to determine the prevalence of MetS were excluded. Also, studies in patients suffering from other clinical diseases were not included.

Results

The meta-analyses of the prevalence (40 studies (n = 6085)) and risk (20 studies (n = 2348)) of MetS in SLE patients were conducted separately. The pooled prevalence of MetS among SLE patients was found to be 26% (95% confidence interval (CI): 22–30%), but varied from 18% (95% CI: 11–25%) to 34% (95% CI: 25–42%), depending upon the diagnostic criteria used. The overall pooled odds ratio (OR) of MetS in SLE patients, compared with healthy controls, was (OR = 2.50; 95% CI: 1.86–3.35), but this ranged from (OR = 1.23; 95% CI: 0.61–2.49) to (OR = 10.71; 95% CI: 1.33–86.48), depending upon the criteria used. Also, the risk of high fasting blood sugar (FBS; OR = 1.59; 95% CI: 1.05–2.40), low high-density lipoprotein cholesterol (HDL-C; OR = 1.43; 95% CI: 1.02–2.01), high blood pressure (BP; OR = 2.76; 95% CI: 2.19–3.47), high triglycerides (TG; OR = 2.85; 95% CI: 2.05–3.95) and high waist circumference (WC; OR = 1.37; 95% CI: 0.97–1.94) were all found to be higher in SLE patients compared with healthy controls.

Conclusions

The risk of MetS was significantly higher in SLE patients, compared with healthy controls, even after adjusting for publication bias. Among MetS components, high TG and high BP were most strongly associated with SLE. Considering that high TG and high BP are preventable, there is an international need to implement effective interventions to reduce MetS components in SLE patients in order to prevent serious outcomes such as cardiovascular diseases and mortality.

Get full access to this article

View all access and purchase options for this article.

References

1. Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and management of the metabolic syndrome. Circulation 2005; 112: 2735–2752.
2. Chung CP, Avalos I, Oeser A, et al. High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: association with disease characteristics and cardiovascular risk factors. Ann Rheum Dis 2007; 66: 208–214.
3. Muniz LF, Pereira RM, Silva TF, Bonfá E, Borba EF. Impact of therapy on metabolic syndrome in young adult premenopausal female lupus patients: beneficial effect of antimalarials. Arthritis Care Res 2015; 67: 1255–1262.
4. Negrón A, Molina M, Mayor A, Rodríguez V, Vilá L. Factors associated with metabolic syndrome in patients with systemic lupus erythematosus from Puerto Rico. Lupus 2008; 17: 348–354.
5. Ward MM. Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum 1999; 42: 338–346.
6. Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 1976; 60: 221–225.
7. Manzi S, Meilahn EN, Rairie JE, et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham study. Am J Epidemiol 1997; 145: 408–415.
8. Sabio J, Zamora-Pasadas M, Jiménez-Jáimez J, et al. Metabolic syndrome in patients with systemic lupus erythematosus from Southern Spain. Lupus 2008; 17: 849–859.
9. Svenungsson E, Jensen-Urstad K, Heimbürger M, et al. Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation 2001; 104: 1887–1893.
10. Bruce IN, Urowitz MB, Gladman DD, Ibañez D, Steiner G. Risk factors for coronary heart disease in women with systemic lupus erythematosus: the Toronto Risk Factor study. Arthritis Rheum 2003; 48: 3159–3167.
11. Sinicato NA, Postal M, de Oliveira PK, Rittner L, Marini R, Appenzeller S. Prevalence and features of metabolic syndrome in childhood-onset systemic lupus erythematosus. Clinical rheumatology 2017; 36: 1527.
12. Das MM, Medeiros C, De Oliveira ÍMaX, Thaysa Á, Ribeiro M. Prevalence of metabolic syndrome in a cohort of systemic lupus erythematosus patients from Northeastern Brazil: association with disease activity, nephritis, smoking, and age. Rheumatology international 2016; 36: 117.
13. Hatef-Fard MR, Khodabandeh M, Sahebari M, Ghayour-Mobarhan M, Rezaieyazdi Z. Metabolic syndrome in lupus patients in northeast of Iran, and their lifestyle habits. Caspian J Internal Med 2016; 7: 195.
14. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6: e1000097.
15. Vandenbroucke JP, Von Elm E, Altman DG, et al. Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. PLoS Med 2007; 4: e297.
16. Modesti PA, Reboldi G, Cappuccio FP, et al. Panethnic differences in blood pressure in Europe: a systematic review and meta-analysis. PLoS One 2016; 11: e0147601.
17. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629–634.
18. Grundy S, Brewer HJ, Cleeman J, Smith JS, Lenfant C. Definition of metabolic syndrome: report of the National Heart, Lung and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004; 109: 433–438.
19. Demir S, Artim-Esen B, Sahinkaya Y, et al. Metabolic syndrome is not only a risk factor for cardiovascular diseases in systemic lupus erythematosus but is also associated with cumulative organ damage: a cross-sectional analysis of 311 patients. Lupus 2016; 25: 177–184.
20. Parker B, Urowitz MB, Gladman DD, et al. Clinical associations of the metabolic syndrome in systemic lupus erythematosus: data from an international inception cohort. Ann Rheum Dis 2013; 72: 1308–1314.
21. Parker B, Urowitz MB, Gladman DD, et al. Impact of early disease factors on metabolic syndrome in systemic lupus erythematosus: data from an international inception cohort. Ann Rheum Dis 2015; 74: 1530–1536.
22. Telles R, Lanna C, Ferreira G, Ribeiro A. Metabolic syndrome in patients with systemic lupus erythematosus: Association with traditional risk factors for coronary heart disease and lupus characteristics. Lupus 2010; 19: 803–809.
23. Liu SY, Han LS, Guo JY, et al. Metabolic syndrome in Chinese patients with systemic lupus erythematosus: no association with plasma cortisol level. Lupus 2013; 22: 519–526.
24. Hatef M, Mirfeizi Z, Sahebari M, Jokar M, Mirheydari M. Superiority of laterally elevated wedged insoles to neutrally wedged insoles in medial knee osteoarthritis symptom relief. Int J Rheum Dis 2014; 17: 84–88.
25. Akarsu S, Ozbagcivan O, Semiz F, Aktan S. High prevalence of metabolic syndrome in patients with discoid lupus erythematosus: a cross-sectional, case-control study. J Immunol Res 2017. doi: 10.1155/2017/3972706.
26. Ormseth MJ, Swift LL, Fazio S, et al. Free fatty acids are associated with metabolic syndrome and insulin resistance but not inflammation in systemic lupus erythematosus. Lupus 2013; 22: 26–33.
27. Das Chagas Medeiros MM, de Oliveira ÍMAX, Ribeiro ÁTM. Prevalence of metabolic syndrome in a cohort of systemic lupus erythematosus patients from Northeastern Brazil: association with disease activity, nephritis, smoking, and age. Rheumatol Int 2016; 36: 117–124.
28. Vadacca M, Margiotta D, Rigon A, et al. Adipokines and systemic lupus erythematosus: relationship with metabolic syndrome and cardiovascular disease risk factors. J Rheumatol 2009; 36: 295–297.
29. Hatef-Fard M, Khodabandeh M, Sahebari M, Ghayour-Mobarhan M, Rezaieyazdi Z. Metabolic syndrome in lupus patients in northeast of Iran, and their lifestyle habits. Caspian J Internal Med 2016; 7: 195–200.
30. Chung C, Avalos I, Oeser A, et al. High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: association with disease characteristics and cardiovascular risk factors. Ann Rheum Dis 2007; 66: 208–214.
31. Parker B, Ahmad Y, Shelmerdine J, et al. An analysis of the metabolic syndrome phenotype in systemic lupus erythematosus. Lupus 2011; 20: 1459–1465.
32. Margiotta D, Navarini L, Vadacca M, et al. Relationship between leptin and regulatory T cells in systemic lupus erythematosus: preliminary results. Eur Rev Med Pharmacol Sci 2016; 20: 636–641.
33. Wang L, Zheng Z, Li T, et al. 25-hydroxyvitamin D is associated with metabolic syndrome among premenopausal women with systemic lupus erythematosus in China. Lupus 2017; 26: 403–409.
34. Sabio J, Vargas-Hitos J, Martinez-Bordonado J, et al. Association between low 25-hydroxyvitamin D, insulin resistance and arterial stiffness in nondiabetic women with systemic lupus erythematosus. Lupus 2015; 24: 155–163.
35. Castejon R, Jimenez-Ortiz C, Rosado S, Tutor-Ureta P, Mellor-Pita S, Yebra-Bango M. Metabolic syndrome is associated with decreased circulating endothelial progenitor cells and increased arterial stiffness in systemic lupus erythematosus. Lupus 2016; 25: 129–136.
36. García-Villegas EA, Lerman-Garber I, Flores-Suárez LF, Aguilar-Salinas C, González HM, Villa-Romero AR. Prognostic value of metabolic syndrome for the development of cardiovascular disease in a cohort of premenopausal women with systemic lupus erythematosus. Medicina Clínica (English Edition) 2015; 144: 289–296.
37. Erdozain JG, Villar I, Nieto J, Ruiz-Irastorza G. Peripheral arterial disease in systemic lupus erythematosus: prevalence and risk factors. J Rheumatol 2014; 41: 310–317.
38. Zhang M, Qi C, Cao L, Qian J, Ni Z. Metabolic syndrome is correlated with carotid atherosclerosis in patients with lupus nephritis. Am J Med Sci 2014; 348: 486–491.
39. Ugarte-Gil MF, Sánchez-Zúñiga C, Gamboa-Cárdenas RV, et al. Circulating naive and memory CD4 + T cells and metabolic syndrome in patients with systemic lupus erythematosus: data from a primarily Mestizo population. Rheumatology 2014; 54: 1302–1307.
40. Kawai VK, Avalos I, Oeser A, et al. Suboptimal inhibition of platelet cyclooxygenase 1 by aspirin in systemic lupus erythematosus: Association with metabolic syndrome. Arthritis Care Res 2014; 66: 285–292.
41. Valero-González S, Castejon R, Jimenez-Ortiz C, et al. Increased arterial stiffness is independently associated with metabolic syndrome and damage index in systemic lupus erythematosus patients. Scand J Rheumatol 2014; 43: 54–58.
42. Gheita T, Raafat H, Sayed S, El-Fishawy H, Nasrallah M, Abdel-Rasheed E. Metabolic syndrome and insulin resistance comorbidity in systemic lupus erythematosus. Zeitschrift Rheumatologie 2013; 72: 172–177.
43. Santos MJ, Pedro LM, Canhão H, et al. Hemorheological parameters are related to subclinical atherosclerosis in systemic lupus erythematosus and rheumatoid arthritis patients. Atherosclerosis 2011; 219: 821–826.
44. Lozovoy MAB, Simao A, Hohmann M, et al. Inflammatory biomarkers and oxidative stress measurements in patients with systemic lupus erythematosus with or without metabolic syndrome. Lupus 2011; 20: 1356–1364.
45. Mok C, Poon W, Lai J, et al. Metabolic syndrome, endothelial injury, and subclinical atherosclerosis in patients with systemic lupus erythematosus. Scand J Rheumatol 2010; 39: 42–49.
46. Sabio J, Vargas-Hitos J, Mediavilla J, et al. Correlation of asymptomatic hyperuricaemia and serum uric acid levels with arterial stiffness in women with systemic lupus erythematosus without clinically evident atherosclerotic cardiovascular disease. Lupus 2010; 19: 591–598.
47. Bellomio V, Spindler A, Lucero E, et al. Metabolic syndrome in Argentinean patients with systemic lupus erythematosus. Lupus 2009; 18: 1019–1025.
48. Zonana-Nacach A, Santana-Sahagún E, Jiménez-Balderas FJ, Camargo-Coronel A. Prevalence and factors associated with metabolic syndrome in patients with rheumatoid arthritis and systemic lupus erythematosus. J Clin Rheumatol 2008; 14: 74–77.
49. Bultink I, Turkstra F, Diamant M, Dijkmans B, Voskuyl A. Prevalence of and risk factors for the metabolic syndrome in women with systemic lupus erythematosus. Clin Exp Rheumatol 2008; 26: 32.
50. El Magadmi M, Ahmad Y, Turkie W, et al. Hyperinsulinemia, insulin resistance, and circulating oxidized low density lipoprotein in women with systemic lupus erythematosus. J Rheumatol 2006; 33: 50–56.

Supplementary Material

Supplementary Material

Lupus

Files in this Data Supplement:

File (appendix1.pdf)

Cite article

Cite article

Cite article

OR

Download to reference manager

If you have citation software installed, you can download article citation data to the citation manager of your choice

Share options

Share

Share this article

Share with email
EMAIL ARTICLE LINK
Share on social media

Share access to this article

Sharing links are not relevant where the article is open access and not available if you do not have a subscription.

For more information view the Sage Journals article sharing page.

Information, rights and permissions

Information

Published In

Pages: 899 - 912
Article first published online: January 4, 2018
Issue published: May 2018

Keywords

  1. Global
  2. metabolic syndrome
  3. prevalence
  4. systemic lupus erythematosus
  5. meta-analysis

Rights and permissions

© The Author(s) 2018.
Request permissions for this article.
PubMed: 29301471

Authors

Affiliations

J Hallajzadeh
Managerial Epidemiology Research Center, Department of Public Health, School of Nursing and Midwifery, Maragheh University of Medical Sciences, Maragheh, Iran
M Khoramdad
Department of Epidemiology and Biostatistics, Faculty of Health, Kermanshah University of Medical Sciences, Kermanshah, Iran
N Izadi
Department of Epidemiology, School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran
N Karamzad
Nutrition Research Center, Department of Biochemistry and Diet Therapy, School of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, Iran
A Almasi-Hashiani
Department of Epidemiology and Reproductive Health, Reproductive Epidemiology Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
E Ayubi
Department of Community Medicine, School of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran
M Qorbani
Non-Communicable Diseases Research Center, Alborz University of Medical Sciences, Karaj, Iran
R Pakzad
Department of Epidemiology, Faculty of Health, Ilam University of Medical Sciences, Ilam, Iran
M J M Sullman
Department of Psychology, Middle East Technical University, Northern Cyprus Campus, Güzelyurt/Morphou, Northern Cyprus
S Safiri
Managerial Epidemiology Research Center, Department of Public Health, School of Nursing and Midwifery, Maragheh University of Medical Sciences, Maragheh, Iran
Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

Notes

S Safiri, Managerial Epidemiology Research Center, Department of Public Health, School of Nursing and Midwifery, Maragheh University of Medical Sciences, North Moallem Street, Maragheh, Iran. Email: [email protected]

Metrics and citations

Metrics

Journals metrics

This article was published in Lupus.

VIEW ALL JOURNAL METRICS

Article usage*

Total views and downloads: 461

*Article usage tracking started in December 2016


Altmetric

See the impact this article is making through the number of times it’s been read, and the Altmetric Score.
Learn more about the Altmetric Scores



Articles citing this one

Receive email alerts when this article is cited

Web of Science: 19 view articles Opens in new tab

Crossref: 20

  1. The global prevalence of gastric cancer in Helicobacter pylori-infecte...
    Go to citation Crossref Google Scholar
  2. Metabolic syndrome in systemic lupus erythematosus patients under Medi...
    Go to citation Crossref Google Scholar
  3. Electromagnetic fields exposure on fetal and childhood abnormalities: ...
    Go to citation Crossref Google Scholar
  4. Older black race is a risk factor for metabolic syndrome in cutaneous ...
    Go to citation Crossref Google ScholarPub Med
  5. Metabolic syndrome in antiphospholipid syndrome versus rheumatoid arth...
    Go to citation Crossref Google Scholar
  6. Prevalence of Pediculosis Among Primary School-Aged Students in Iran: ...
    Go to citation Crossref Google Scholar
  7. Association of body composition in early pregnancy with gestational di...
    Go to citation Crossref Google Scholar
  8. Development of High Fat Diet-Induced Hyperinsulinemia in Mice Is Enhan...
    Go to citation Crossref Google Scholar
  9. Global and Regional Prevalence of Diabetic Retinopathy; A Comprehensiv...
    Go to citation Crossref Google Scholar
  10. Redox Homeostasis Involvement in the Pharmacological Effects of Metfor...
    Go to citation Crossref Google Scholar
  11. Worldwide prevalence of fungal coinfections among COVID-19 patients: a...
    Go to citation Crossref Google Scholar
  12. Metabolic Syndrome: Dermatological Aspects in Women
    Go to citation Crossref Google Scholar
  13. Worldwide prevalence of microbial agents’ coinfection among COVID‐19 p...
    Go to citation Crossref Google Scholar
  14. Effect of gestational diabetes mellitus on lipid profile: A systematic...
    Go to citation Crossref Google Scholar
  15. Type II diabetes mellitus risk assessment using FINDRISC questionnaire...
    Go to citation Crossref Google Scholar
  16. Metabolic determinants of lupus pathogenesis
    Go to citation Crossref Google Scholar
  17. Skin disease related to metabolic syndrome in women
    Go to citation Crossref Google Scholar
  18. Correlation between Osteoprotegerin Levels and Antiphospholipid Syndro...
    Go to citation Crossref Google Scholar
  19. Serum osteopontin negatively impacts on intima‐media thickness in pati...
    Go to citation Crossref Google Scholar

Figures and tables

Figures & Media

Tables

View Options

Get access

Access options

If you have access to journal content via a personal subscription, university, library, employer or society, select from the options below:


Alternatively, view purchase options below:

Purchase 24 hour online access to view and download content.

Access journal content via a DeepDyve subscription or find out more about this option.

View options

PDF/ePub

View PDF/ePub

Full Text

View Full Text