677
Views
30
CrossRef citations to date
0
Altmetric
Review

Metabolic syndrome and systemic lupus erythematosus: the connection

ORCID Icon
Pages 765-775 | Received 16 Feb 2019, Accepted 15 May 2019, Published online: 27 May 2019

References

  • Cameron A. The metabolic syndrome: validity and utility of clinical definitions for cardiovascular disease and diabetes risk prediction. Maturitas. 2010;65:117–121.
  • Isomaa B, Almgren P, Tuomi T, et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 2001;24:683–689.
  • Alexander CM, Landsman PB, Teutsch SM, et al. Third National Health and Nutrition Examination Survey (NHANES III); National Cholesterol Education Program (NCEP). NCEP-defined metabolic syndrome, diabetes, and prevalence of coronary heart disease among NHANES III participants age 50 years and older. Diabetes. 2003;52:1210–1214.
  • Wong ND, Nelson JC, Granston T, et al. Metabolic syndrome, diabetes, and incidence and progression of coronary calcium: the Multiethnic Study of Atherosclerosis study. JACC Cardiovasc Imaging. 2012;5:358–366.
  • Thomas GN, Schooling CM, McGhee SM, et al. Hong Kong cardiovascular risk factor prevalence study steering committee. Metabolic syndrome increases all-cause and vascular mortality: the Hong Kong Cardiovascular Risk Factor Study. Clin Endocrinol (Oxf). 2007;66:666–671.
  • Mottillo S, Filion KB, Genest J, et al. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol. 2010;56:1113–1132.
  • Li W, Ma D, Liu M, et al. Association between metabolic syndrome and risk of stroke: a meta-analysis of cohort studies. Cerebrovasc Dis. 2008;25:539–547.
  • Novo S, Peritore A, Guarneri FP, et al. Metabolic syndrome (MetS) predicts cardio and cerebrovascular events in a twenty years follow-up. A prospective study. Atherosclerosis. 2012;223:468–472.
  • Wu SH, Liu Z, Ho SC, et al. Metabolic syndrome and all-cause mortality: a meta-analysis of prospective cohort studies. Eur J Epidemiol. 2010;25:375–384.
  • Gami AS, Witt BJ, Howard DE, et al. Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies. J Am Coll Cardiol. 2007;49:403–414.
  • Ju SY, Lee JY, Kim DH. Association of metabolic syndrome and its components with all-cause and cardiovascular mortality in the elderly: A meta-analysis of prospective cohort studies. Medicine (Baltimore). 2017;96:e8491.
  • Hess PL, Al-Khalidi HR, Friedman DJ, et al. The Metabolic syndrome and risk of sudden cardiac death: the atherosclerosis risk in communities study. J Am Heart Assoc. 2017;6:e006103.
  • Ma X, Zhu S. Metabolic syndrome in the prevention of cardiovascular diseases and diabetes–still a matter of debate? Eur J Clin Nutr. 2013;67:518–521.
  • Yen YF, Hu HY, Lin IF, et al. Associations of Metabolic Syndrome and its Components With Mortality in the Elderly: A Cohort Study of 73,547 Taiwanese Adults. Medicine (Baltimore). 2015;94:e956.
  • van Herpt TT, Dehghan A, van Hoek M, et al. The clinical value of metabolic syndrome and risks of cardiometabolic events and mortality in the elderly: the Rotterdam study. Cardiovasc Diabetol. 2016 Apr;27(15):69.
  • Chen Q, Zhang Y, Ding D, et al. Metabolic syndrome and its individual components with mortality among patients with coronary heart disease. Int J Cardiol. 2016;224:8–14.
  • Grandl G, Wolfrum C. Hemostasis, endothelial stress, inflammation, and the metabolic syndrome. Semin Immunopathol. 2018;40:215–224.
  • Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest. 2011;121:2111–2117.
  • Abella V, Scotece M, Conde J, et al. Adipokines, metabolic syndrome and rheumatic diseases. J Immunol Res. 2014;2014:343746.
  • Medina G, Vera-Lastra O, Peralta-Amaro AL, et al. Metabolic syndrome, autoimmunity and rheumatic diseases. Pharmacol Res. 2018 Jul;133:277–288.
  • Frühbeck G, Catalán V, Rodríguez A, et al. Involvement of the leptin-adiponectin axis in inflammation and oxidative stress in the metabolic syndrome. Sci Rep. 2017;7:6619.
  • McCracken E, Monaghan M, Sreenivasan S. Pathophysiology of the metabolic syndrome. Clin Dermatol. 2018;36:14–20.
  • Van Raemdonck K, Umar S, Szekanecz Z, et al. Impact of obesity on autoimmune arthritis and its cardiovascular complications. Autoimmun Rev. 2018;17:821–835.
  • Mok CC. Systemic lupus erythematosus: what should family physicians know in 2018? Hong Kong Med J. 2018;24:501–511.
  • Mok CC. The Jakinibs in systemic lupus erythematosus: progress and prospects. Expert Opin Investig Drugs. 2019;28:85–92.
  • Mok CC. Accelerated atherosclerosis, arterial thromboembolism, and preventive strategies in systemic lupus erythematosus. Scand J Rheumatol. 2006;35:85–95.
  • Croca S, Rahman A. Atherosclerosis in systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2017;31:364–372.
  • Sun C, Qin W, Zhang Y-H, et al. Prevalence and risk of metabolic syndrome in patients with systemic lupus erythematosus: A meta-analysis. Int J Rheum Dis. 2017;20:917–928.
  • Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998;15:539–553.
  • National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). 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) final report. Circulation. 2002;106:3143–3421.
  • Alberti KG, Zimmet P, Shaw J. IDF Epidemiology Task Force Consensus Group. The metabolic syndrome–a new worldwide definition. Lancet. 2005;366:1059–1062.
  • Balkau B, Charles MA. Comment on the provisional report from the WHO consultation. European Group for the Study of Insulin Resistance (EGIR). Diabet Med. 1999;16:442–443.
  • Bloomgarden ZT. American Association of Clinical Endocrinologists (AACE) consensus conference on the insulin resistance syndrome: 25-26 August 2002, Washington, DC. Diabetes Care. 2003;26:1297–1303.
  • Alberti KG, Eckel RH, Grundy SMZ, et al. International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Circulation. 2009;120:1640–1645.
  • Heng D, Ma S, Lee JJ, et al. Modification of the NCEP ATP III definitions of the metabolic syndrome for use in Asians identifies individuals at risk of ischemic heart disease. Atherosclerosis. 2006;186:367–373.
  • Katz P, Gregorich S, Yazdany J, et al. Obesity and its measurement in a community-based sample of women with systemic lupus erythematosus. Arthritis Care Res (Hoboken). 2011;63:261–268.
  • Versini M, Tiosano S, Comaneshter D, et al. Smoking and obesity in systemic lupus erythematosus: a cross-sectional study. Eur J Clin Invest. 2017;47:422–427.
  • Patterson SL, Schmajuk G, Jafri K, et al. Obesity is independently associated with worse patient-reported outcomes in women with systemic lupus erythematosus. Arthritis Care Res (Hoboken). 2019;71:126–133.
  • Tedeschi SK, Barbhaiya M, Malspeis S, et al. Obesity and the risk of systemic lupus erythematosus among women in the Nurses’ Health Studies. Semin Arthritis Rheum. 2017;47:376–383.
  • Cozier YC, Barbhaiya M, Castro-Webb N, et al. A prospective study of obesity and risk of systemic lupus erythematosus (SLE) among Black women. Semin Arthritis Rheum. 2018;S0049-0172(18)30425–6.
  • Katz P, Julian L, Tonner MC, et al. Physical activity, obesity, and cognitive impairment among women with systemic lupus erythematosus. Arthritis Care Res (Hoboken). 2012;64:502–510.
  • Oeser A, Chung CP, Asanuma Y, et al. Obesity is an independent contributor to functional capacity and inflammation in systemic lupus erythematosus. Arthritis Rheum. 2005;52:3651–3659.
  • Mok CC, Ying SK, To CH, et al. Bone mineral density and body composition in men with systemic lupus erythematosus: a case control study. Bone. 2008;43:327–331.
  • Szabó MZ, Szodoray P, Kiss E. Dyslipidemia in systemic lupus erythematosus. Immunol Res. 2017;65:543–550.
  • Tselios K, Koumaras C, Gladman D, et al. Dyslipidemia in systemic lupus erythematosus: just another comorbidity?. Semin Arthritis Rheum. 2016;45:604–610.
  • Borba EF, Bonfá E. Dyslipoproteinemias in systemic lupus erythematosus: influence of disease, activity, and anticardiolipin antibodies. Lupus. 1997;6:533–539.
  • Tyrrell PN, Beyene J, Benseler SM, et al. Predictors of lipid abnormalities in children with new-onset systemic lupus erythematosus. J Rheumatol. 2007;34:2112–2119.
  • Al-Herz A, Ensworth S, Shojania K, et al. Cardiovascular risk factor screening in systemic lupus erythematosus. J Rheumatol. 2003;30:493–496.
  • Sabio JM, Vargas-Hitos JA, Navarrete-Navarrete N, et al. Prevalence of and factors associated with hypertension in young and old women with systemic lupus erythematosus. J Rheumatol. 2011;38:1026–1032.
  • Shaharir SS, Mustafar R, Mohd R, et al. Persistent hypertension in lupus nephritis and the associated risk factors. Clin Rheumatol. 2015;34:93–97.
  • Wolf VL, Ryan MJ. Autoimmune Disease-Associated Hypertension. Curr Hypertens Rep. 2019;21:10.
  • Sabio JM, Vargas-Hitos JA, Martínez Bordonado J, et al. Association between non-dipper hypertension and vitamin D deficiency in women with systemic lupus erythematosus. Clin Exp Rheumatol. 2019;37:286–292.
  • Ramirez LA, Sullivan JC. Sex Differences in Hypertension: where We Have Been and Where We Are Going. Am J Hypertens. 2018;31:1247–1254.
  • Bravo PE, Morse S, Borne DM, et al. Leptin and hypertension in obesity. Vasc Health Risk Manag. 2006;2:163–169.
  • Li HM, Zhang TP, Leng RX, et al. Emerging role of adipokines in systemic lupus erythematosus. Immunol Res. 2016;64:820–830.
  • Ryan MJ, McLemore GR Jr, St H. Insulin resistance and obesity in a mouse model of systemic lupus erythematosus. Hypertension. 2006;48:988–993.
  • Toller-Kawahisa JE, Canicoba N, Venancio V, et al. Systemic lupus erythematosus onset in lupus-prone B6.MRL/lpr mice Is influenced by weight gain and Is preceded by an increase in neutrophil oxidative burst activity. Free Radic Biol Med. 2015;86:362–373.
  • 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.
  • Chung CP, Oeser A, Solus JF, et al. Inflammation-associated insulin resistance: differential effects in rheumatoid arthritis and systemic lupus erythematosus define potential mechanisms. Arthritis Rheum. 2008;58:2105–2112.
  • Miyake CNH, Gualano B, Dantas WS, et al. Increased insulin resistance and glucagon levels in mild/inactive systemic lupus erythematosus patients despite normal glucose tolerance. Arthritis Care Res (Hoboken). 2018;70:114–124.
  • Sánchez-Pérez H, Tejera-Segura B, de Vera-González A, et al. Insulin resistance in systemic lupus erythematosus patients: contributing factors and relationship with subclinical atherosclerosis. Clin Exp Rheumatol. 2017;35:885–892.
  • Sabio JM, Vargas-Hitos JA, 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.
  • Lozovoy MA, Simão AN, Oliveira SR, et al. Relationship between iron metabolism, oxidative stress, and insulin resistance in patients with systemic lupus erythematosus. Scand J Rheumatol. 2013;42:303–310.
  • Parker B, Bruce I. SLE and metabolic syndrome. Lupus. 2013;22:1259–1266.
  • Parker B, Ahmad Y, Shelmerdine J, et al. An analysis of the metabolic syndrome phenotype in systemic lupus erythematosus. Lupus. 2011;20:1459–1465.
  • Sabio JM, Zamora-Pasadas M, Jime´ nez-Ja´ Imez J, et al. Metabolic syndrome in patients with systemic lupus erythematosus from Southern Spain. Lupus. 2008;17:849–859.
  • Hallajzadeh J, Khoramdad M, Izadi N, et al. The association between metabolic syndrome and its components with systemic lupus erythematosus: a comprehensive systematic review and meta-analysis of observational studies. Lupus. 2018;1:961203317751047.
  • 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.
  • Bellomio V, Spindler A, Lucero E, et al. SLE study group of the argentinean society of rheumatology. Metabolic syndrome in Argentinean patients with systemic lupus erythematosus. Lupus. 2009;18:1019–1025.
  • Negrón AM, Molina MJ, Mayor AM, et al. Factors associated with metabolic syndrome in patients with systemic lupus erythematosus from Puerto Rico. Lupus. 2008;17:348–354.
  • Mok CC, Poon WL, Lai JP, et al. Metabolic syndrome, endothelial injury, and subclinical atherosclerosis in patients with systemic lupus erythematosus. Scand J Rheumatol. 2010;39:42–49.
  • 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.
  • Muniz LF, Pereira RM, Silva TF, et al. Impact of therapy on metabolic syndrome in young adult premenopausal female lupus patients: beneficial effect of antimalarials. Arthritis Care Res (Hoboken). 2015;67:1255–1262.
  • Medeiros MM, Xavier de Oliveira ÍM, Ribeiro ÁT. 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.
  • Wang LM, Zheng ZH, Li TF, et al. 25-hydroxyvitamin D is associated with metabolic syndrome among premenopausal women with systemic lupus erythematosus in China. Lupus. 2017;26:403–409.
  • Demir S, Erten G, Artım-Esen B, et al. Increased serum leptin levels are associated with metabolic syndrome and carotid intima media thickness in premenopausal systemic lupus erythematosus patients without clinical atherosclerotic vascular events. Lupus. 2018;27:1509–1516.
  • Mobini M, Niksolat F, Mohammadpour RA, et al. Metabolic syndrome in patients with systemic lupus erythematosus: association with disease activity, disease damage and age. Int J Rheum Dis. 2018;21:1023–1030.
  • Fatemi A, Ghanbarian A, Sayedbonakdar Z, et al. Metabolic syndrome in Iranian patients with systemic lupus erythematosus and its determinants. Clin Rheumatol. 2018;37:1521–1528.
  • Mok CC, Tse SM, Chan KL, et al. Effect of the metabolic syndrome on organ damage and mortality in patients with systemic lupus erythematosus: a longitudinal analysis. Clin Exp Rheumatol. 2018;36:389–395.
  • Da Rosa Franchi Santos LF, Stadtlober NP, Costa Dall’Aqua LG, et al. Increased adhesion molecule levels in systemic lupus erythematosus: relationships with severity of illness, autoimmunity, metabolic syndrome and cortisol levels. Lupus. 2018;27:380–388.
  • Conti F, Ceccarelli F, Perricone C, et al. The chronic damage in systemic lupus erythematosus is driven by flares, glucocorticoids and antiphospholipid antibodies: results from a monocentric cohort. Lupus. 2016 Jun;25(7):719–726.
  • Tarr T, Papp G, Nagy N, et al. Chronic high-dose glucocorticoid therapy triggers the development of chronic organ damage and worsens disease outcome in systemic lupus erythematosus. Clin Rheumatol. 2017 Feb;36(2):327–333.
  • Chen HL, Shen LJ, Hsu PN, et al. Cumulative burden of glucocorticoid-related adverse events in patients with systemic lupus erythematosus: findings from a 12-year longitudinal study. J Rheumatol. 2018;45:83–89.
  • Petri M. Detection of coronary artery disease and the role of traditional risk factors in the Hopkins Lupus Cohort. Lupus. 2000;9(3):170–175.
  • Magder LS, Petri M. Incidence of and risk factors for adverse cardiovascular events among patients with systemic lupus erythematosus. Am J Epidemiol. 2012;176:708–719.
  • Sabio JM, Vargas-Hitos J, Zamora-Pasadas M, et al. Metabolic syndrome is associated with increased arterial stiffness and biomarkers of subclinical atherosclerosis in patients with systemic lupus erythematosus. J Rheumatol. 2009;36:2204–2211.
  • Valero-Gonzalez 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.
  • Castejon R, Jimenez-Ortiz C, Rosado S, et al. Metabolic syndrome is associated with decreased circulating endothelial progenitor cells and increased arterial stiffness in systemic lupus erythematosus. Lupus. 2016;25:129–136.
  • Gheita TA, Raafat HA, Sayed S, et al. Metabolic syndrome and insulin resistance comorbidity in systemic lupus erythematosus. Effect on carotid intima-media thickness. Z Rheumatol. 2013;72:172–177.
  • Zhang M, Qi C, Cao L, et al. Metabolic syndrome is correlated with carotid atherosclerosis in patients with lupus nephritis. Am J Med Sci. 2014;348:486–491.
  • García-Villegas EA, Lerman-Garber I, Flores-Suárez LF, et al. Prognostic value of metabolic syndrome for the development of cardiovascular disease in a cohort of premenopausal women with systemic lupus erythematosus. Med Clin (Barc). 2015;144:289–296.
  • Demir S, Artim-Esen B, Şahinkaya 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.
  • Margiotta DPE, Basta F, Dolcini G, et al. The relation between, metabolic syndrome and quality of life in patients with Systemic Lupus Erythematosus. PLoS One. 2017;12:e0187645.
  • Lee JW, Kang JH, Lee KE, et al. Effects of risk factors for and components of metabolic syndrome on the quality of life of patients with systemic lupus erythematosus: a structural equation modeling approach. Qual Life Res. 2018;27:105–113.
  • Prasad GV. Metabolic syndrome and chronic kidney disease: current status and future directions. World J Nephrol. 2014;3:210–219.
  • Thomas G1, Sehgal AR, Kashyap SR, et al. Metabolic syndrome and kidney disease: a systematic review and meta-analysis. Clin J Am Soc Nephrol. 2011;6:2364–2373.
  • Chen J, Muntner P, Hamm LL, et al. The metabolic syndrome and chronic kidney disease in U.S. Adults Ann Intern Med. 2004;140:167–174.
  • Pons-Estel GJ, Andreoli L, Scanzi F, et al. The antiphospholipid syndrome in patients with systemic lupus erythematosus. J Autoimmun. 2017;76:10–20.
  • Rodrigues CE, Bonfá E, Caleiro MT, et al. Association of arterial events with the coexistence of metabolic syndrome and primary antiphospholipid syndrome. Arthritis Care Res (Hoboken). 2012;64:1576–1583.
  • Medina G, Gutiérrez-Moreno AL, Vera-Lastra O, et al. Prevalence of metabolic syndrome in primary antiphospholipid syndrome patients. Autoimmun Rev. 2011;10:214–217.
  • Rodrigues CE, Vendramini MB, Bueno C, et al. Adipocytokines in primary antiphospholipid syndrome: potential markers of low-grade inflammation, insulin resistance and metabolic syndrome. Clin Exp Rheumatol. 2012;30:871–878.
  • Kaur J. A comprehensive review on metabolic syndrome. Cardiol Res Pract. 2014;2014:943162.
  • Bell-Anderson KS. Adipokines: linking obesity and cardiovascular disease. Expert Rev Endocrinol Metab. 2008;3:61–73.
  • Zhu Q, Scherer PE. Immunologic and endocrine functions of adipose tissue: implications for kidney disease. Nat Rev Nephrol. 2018;14:105–120.
  • Bao P, Liu G, Wei Y. Association between IL-6 and related risk factors of metabolic syndrome and cardiovascular disease in young rats. Int J Clin Exp Med. 2015;8:13491–13499.
  • McKellar GE, McCarey DW, Sattar N, et al. Role for TNF in atherosclerosis? Lessons from autoimmune disease. Nat Rev Cardiol. 2009;6:410–417.
  • Kern PA, Ranganathan S, Li C, et al. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab. 2001;280:E745–E751.
  • Alessi MC, Juhan-Vague I. PAI-1 and the metabolic syndrome: links, causes, and consequences. Arterioscler Thromb Vasc Biol. 2006;26:2200–2207.
  • Furukawa S, Fujita T, Shimabukuro M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752–1761.
  • Chung CP, Long AG, Solus JF, et al. Adipocytokines in systemic lupus erythematosus: relationship to inflammation, insulin resistance and coronary atherosclerosis. Lupus. 2009;18:799–806.
  • 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.
  • McMahon M, Skaggs BJ, Sahakian L, et al. High plasma leptin levels confer increased risk of atherosclerosis in women with systemic lupus erythematosus, and are associated with inflammatory oxidised lipids. Ann Rheum Dis. 2011;70:1619–1624.
  • Wang X, Qiao Y, Yang L, et al. Leptin levels in patients with systemic lupus erythematosus inversely correlate with regulatory T cell frequency. Lupus. 2017;26:1401–1406.
  • De Sanctis JB, Zabaleta M, Bianco NE, et al. Serum adipokine levels in patients with systemic lupus erythematosus. Autoimmunity. 2009;42:272–274.
  • Wisłowska M, Rok M, Stepień K, et al. Serum leptin in systemic lupus erythematosus. Rheumatol Int. 2008;28:467–473.
  • Li HM, Zhang TP, Leng RX, et al. Plasma/Serum leptin levels in patients with systemic lupus erythematosus: a meta-analysis. Arch Med Res. 2015;46:551–556.
  • Katsiki N, Mantzoros C, Mikhailidis DP. Adiponectin, lipids and atherosclerosis. Curr Opin Lipidol. 2017;28:347–354.
  • Matsuzawa Y, Funahashi T, Kihara S, et al. Adiponectin and metabolic syndrome. Arterioscler Thromb Vasc Biol. 2004;24:29–33.
  • Srikanthan K, Feyh A, Visweshwar H, et al. Systematic review of metabolic syndrome biomarkers: a panel for early detection, management, and risk stratification in the West Virginian population. Int J Med Sci. 2016;13:25–38.
  • Ryo M, Nakamura T, Kihara S, et al. Adiponectin as a biomarker of the metabolic syndrome. Circ J. 2004;68:975–981.
  • Dini AA, Wang P, Ye D-Q. Serum Adiponectin Levels in Patients With Systemic Lupus Erythematosus: A Meta-analysis. J Clin Rheumatol. 2017;23:361–367.
  • Huang Q, Tao -S-S, Zhang Y-J, et al. Serum resistin levels in patients with rheumatoid arthritis and systemic lupus erythematosus: a meta-analysis. Clin Rheumatol. 2015;34:1713–1720.
  • Chougule D, Nadkar M, Venkataraman K, et al. Adipokine interactions promote the pathogenesis of systemic lupus erythematosus. Cytokine. 2018;111:20–27.
  • Dimitroulas T, Sandoo A, Kitas GD. Asymmetric dimethylarginine as a surrogate marker of endothelial dysfunction and cardiovascular risk in patients with systemic rheumatic diseases. Int J Mol Sci. 2012;13:12315–12335.
  • Siervo M, Bluck LJ. In vivo nitric oxide synthesis, insulin sensitivity, and asymmetric dimethylarginine in obese subjects without and with metabolic syndrome. Metabolism. 2012;61:680–688.
  • Perna M, Roman MJ, Alpert DR, et al. Relationship of asymmetric dimethylarginine and homocysteine to vascular aging in systemic lupus erythematosus patients. Arthritis Rheum. 2010;62:1718–1722.
  • Kiani AN, Mahoney JA, Petri M. Asymmetric dimethylarginine is a marker of poor prognosis and coronary calcium in systemic lupus erythematosus. J Rheumatol. 2007;34:1502–1505.
  • Torres S, Fabersani E, Marquez A, et al. Adipose tissue inflammation and metabolic syndrome. The proactive role of probiotics. Eur J Nutr. 2018 Jul 24. DOI:10.1007/s00394-018-1790-2 [Epub ahead of print].
  • de Oliveira GLV, Leite AZ, Higuchi BS, et al. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology. 2017;152:1–12.
  • Katz-Agranov N, Zandman-Goddard G. The microbiome and systemic lupus erythematosus. Immunol Res. 2017;65:432–437.
  • Yamaoka K, Tango T. Effects of lifestyle modification on metabolic syndrome: a systematic review and meta-analysis. BMC Med. 2012;10:138.
  • Grundy SM, Stone NJ, Bailey AL, et al. AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA guideline on the management of blood cholesterol: a report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines. J Am Coll Cardiol. 2018 Nov 8;2018:S0735-1097(18)39034-X. [Epub ahead of print].
  • Rask Larsen J, Dima L, Correll CU, et al. The pharmacological management of metabolic syndrome. Expert Rev Clin Pharmacol. 2018;11:397–410.
  • Okopień B, Bułdak Ł, Bołdys A. Benefits and risks of the treatment with fibrates–a comprehensive summary. Expert Rev Clin Pharmacol. 2018;11:1099–1112.
  • Ladeiras-Lopes R, Fontes-Carvalho R, Bettencourt N, et al. Novel therapeutic targets of metformin: metabolic syndrome and cardiovascular disease. Expert Opin Ther Targets. 2015;19:869–877.
  • Varjabedian L, Bourji M, Pourafkari L, et al. Cardioprotection by Metformin: beneficial Effects Beyond Glucose Reduction. Am J Cardiovasc Drugs. 2018;18:181–193.
  • Zinman B, Wanner C, Lachin JM, et al. EMPA-REG OUTCOME Investigators. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med. 2015;373:2117–2128.
  • Marso SP, Daniels GH, Brown-Frandsen K, et al. Investigators. Liraglutide and Cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2016;375:311–322.
  • Floris A, Piga M, Mangoni AA, et al. Protective effects of hydroxychloroquine against accelerated atherosclerosis in systemic lupus erythematosus. Mediators Inflamm. 2018;2018:3424136. eCollection 2018.
  • Rempenault C, Combe B, Barnetche T, et al. Metabolic and cardiovascular benefits of hydroxychloroquine in patients with rheumatoid arthritis: a systematic review and meta-analysis. Ann Rheum Dis. 2018;77:98–103.
  • Bertsias GK, Tektonidou M, Amoura Z, et al. Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann Rheum Dis. 2012;71:1771–1782.
  • Fanouriakis A, Kostopoulou M, Alunno A, et al. update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis. 2019 Mar 29;2019:annrheumdis-2019–215089. [Epub ahead of print].

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.