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

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.

[1]  H. Nam,et al.  25-Hydroxyvitamin D Is Associated with Kidney Function: The Dong-gu Study. , 2018, Journal of nutritional science and vitaminology.

[2]  L. Rittner,et al.  Prevalence and features of metabolic syndrome in childhood-onset systemic lupus erythematosus , 2017, Clinical Rheumatology.

[3]  L-M Wang,et al.  25-hydroxyvitamin D is associated with metabolic syndrome among premenopausal women with systemic lupus erythematosus in China , 2017, Lupus.

[4]  Ş. Aktan,et al.  High Prevalence of Metabolic Syndrome in Patients with Discoid Lupus Erythematosus: A Cross-Sectional, Case-Control Study , 2017, Journal of immunology research.

[5]  M. Ghayour-Mobarhan,et al.  Metabolic syndrome in lupus patients in northeast of Iran, and their lifestyle habits. , 2016, Caspian journal of internal medicine.

[6]  M. Inanç,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 , 2016, Lupus.

[7]  C. Jimenez-Ortiz,et al.  Metabolic syndrome is associated with decreased circulating endothelial progenitor cells and increased arterial stiffness in systemic lupus erythematosus , 2016, Lupus.

[8]  G. Parati,et al.  Panethnic Differences in Blood Pressure in Europe: A Systematic Review and Meta-Analysis , 2016, PloS one.

[9]  E. Bonfá,et al.  Impact of Therapy on Metabolic Syndrome in Young Adult Premenopausal Female Lupus Patients: Beneficial Effect of Antimalarials , 2015, Arthritis care & research.

[10]  G. Alarcón,et al.  Circulating naive and memory CD4+ T cells and metabolic syndrome in patients with systemic lupus erythematosus: data from a primarily Mestizo population. , 2015, Rheumatology.

[11]  Carlos Aguilar-Salinas,et al.  Prognostic value of metabolic syndrome for the development of cardiovascular disease in a cohort of premenopausal women with systemic lupus erythematosus. , 2015, Medicina clinica.

[12]  J. Sabio,et al.  Association between low 25-hydroxyvitamin D, insulin resistance and arterial stiffness in nondiabetic women with systemic lupus erythematosus , 2015, Lupus.

[13]  Z. Ni,et al.  Metabolic Syndrome Is Correlated With Carotid Atherosclerosis in Patients With Lupus Nephritis , 2014, The American journal of the medical sciences.

[14]  I. Bruce,et al.  Impact of early disease factors on metabolic syndrome in systemic lupus erythematosus: data from an international inception cohort , 2014, Annals of the rheumatic diseases.

[15]  J. Oates,et al.  Suboptimal Inhibition of Platelet Cyclooxygenase 1 by Aspirin in Systemic Lupus Erythematosus: Association With Metabolic Syndrome , 2014, Arthritis care & research.

[16]  G. Ruiz-Irastorza,et al.  Peripheral Arterial Disease in Systemic Lupus Erythematosus: Prevalence and Risk Factors , 2014, The Journal of Rheumatology.

[17]  C. Jimenez-Ortiz,et al.  Increased arterial stiffness is independently associated with metabolic syndrome and damage index in systemic lupus erythematosus patients , 2014, Scandinavian journal of rheumatology.

[18]  Z. Mirfeizi,et al.  Superiority of laterally elevated wedged insoles to neutrally wedged insoles in medial knee osteoarthritis symptom relief , 2014, International journal of rheumatic diseases.

[19]  Xin Zhang,et al.  Metabolic syndrome in Chinese patients with systemic lupus erythematosus: no association with plasma cortisol level , 2013, Lupus.

[20]  T. Gheita,et al.  Metabolic syndrome and insulin resistance comorbidity in systemic lupus erythematosus , 2013, Zeitschrift für Rheumatologie.

[21]  P. Raggi,et al.  Free fatty acids are associated with metabolic syndrome and insulin resistance but not inflammation in systemic lupus erythematosus , 2013, Lupus.

[22]  I. Bruce,et al.  Clinical associations of the metabolic syndrome in systemic lupus erythematosus: data from an international inception cohort , 2012, Annals of the rheumatic diseases.

[23]  M. Santos,et al.  Hemorheological parameters are related to subclinical atherosclerosis in systemic lupus erythematosus and rheumatoid arthritis patients. , 2011, Atherosclerosis.

[24]  I. Bruce,et al.  An analysis of the metabolic syndrome phenotype in systemic lupus erythematosus , 2011, Lupus.

[25]  R. Cecchini,et al.  Inflammatory biomarkers and oxidative stress measurements in patients with systemic lupus erythematosus with or without metabolic syndrome , 2011, Lupus.

[26]  R. Telles,et al.  Metabolic syndrome in patients with systemic lupus erythematosus: association with traditional risk factors for coronary heart disease and lupus characteristics , 2010, Lupus.

[27]  J. Sabio,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 , 2010, Lupus.

[28]  G. Ko,et al.  Metabolic syndrome, endothelial injury, and subclinical atherosclerosis in patients with systemic lupus erythematosus , 2010, Scandinavian journal of rheumatology.

[29]  A. Berman,et al.  Metabolic syndrome in Argentinean patients with systemic lupus erythematosus , 2009, Lupus.

[30]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement , 2009, BMJ.

[31]  F. Cacciapaglia,et al.  Adipokines and Systemic Lupus Erythematosus: Relationship with Metabolic Syndrome and Cardiovascular Disease Risk Factors , 2009, The Journal of Rheumatology.

[32]  M. González-Gay,et al.  Metabolic syndrome in patients with systemic lupus erythematosus from Southern Spain , 2008, Lupus.

[33]  E. Santana-Sahagún,et al.  Prevalence and Factors Associated With Metabolic Syndrome in Patients With Rheumatoid Arthritis and Systemic Lupus Erythematosus , 2008, Journal of clinical rheumatology : practical reports on rheumatic & musculoskeletal diseases.

[34]  V. Rodríguez,et al.  Factors associated with metabolic syndrome in patients with systemic lupus erythematosus from Puerto Rico , 2008, Lupus.

[35]  S. Pocock,et al.  Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): Explanation and Elaboration , 2007, Epidemiology.

[36]  P. Raggi,et al.  High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: association with disease characteristics and cardiovascular risk factors , 2006, Annals of the rheumatic diseases.

[37]  Fernando Costa,et al.  Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. , 2005, Circulation.

[38]  Claude Lenfant,et al.  Definition of Metabolic Syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association Conference on Scientific Issues Related to Definition , 2004, Arteriosclerosis, thrombosis, and vascular biology.

[39]  I. Bruce,et al.  Risk factors for coronary heart disease in women with systemic lupus erythematosus: the Toronto Risk Factor Study. , 2003, Arthritis and rheumatism.

[40]  A. Hamsten,et al.  Risk Factors for Cardiovascular Disease in Systemic Lupus Erythematosus , 2001, Circulation.

[41]  M. Ward Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. , 1999, Arthritis and rheumatism.

[42]  G. Smith,et al.  Bias in meta-analysis detected by a simple, graphical test , 1997, BMJ.

[43]  R. D'Agostino,et al.  Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. , 1997, American journal of epidemiology.

[44]  M. Urowitz,et al.  The bimodal mortality pattern of systemic lupus erythematosus. , 1976, The American journal of medicine.

[45]  Y. Takahashi [Free fatty acids]. , 1967, Nihon rinsho. Japanese journal of clinical medicine.

[46]  L. Metzger Superiority of laterally elevated wedged insoles to neutrally wedged insoles in medial knee osteoarthritis symptom relief , 2016 .

[47]  A. Afeltra,et al.  Relationship between leptin and regulatory T cells in systemic lupus erythematosus: preliminary results. , 2016, European review for medical and pharmacological sciences.

[48]  M. Medeiros,et al.  Prevalence of metabolic syndrome in a cohort of systemic lupus erythematosus patients from Northeastern Brazil: association with disease activity, nephritis, smoking, and age , 2015, Rheumatology International.

[49]  B. Dijkmans,et al.  Prevalence of and risk factors for the metabolic syndrome in women with systemic lupus erythematosus. , 2008, Clinical and experimental rheumatology.

[50]  I. Bruce,et al.  Hyperinsulinemia, insulin resistance, and circulating oxidized low density lipoprotein in women with systemic lupus erythematosus. , 2006, Journal of Rheumatology.

[51]  H. Minuk,et al.  Metabolic syndrome. , 2005, Journal of insurance medicine.

[52]  R. Krauss,et al.  Diagnosis and management of the metabolic syndrome , 2005 .