Insulin Resistance and Diabetes Mellitus in Patients with Systemic Lupus
Erythematosus

Mario      García-Carrasco; Claudia      Mendoza-Pinto; Pamela      Munguía-Realpozo; Ivet      Etchegaray-Morales; Sandra Karina      Vélez-Pelcastre; Socorro      Méndez-Martínez; Irma      Zamora-Ginez; Luis Guillermo   Vázquez   de Lara; José Luis      Gálvez-Romero; Marco      Escamilla-Márquez
doi:10.2174/1871530322666220908154253
Abstract

Systemic lupus erythematosus (SLE) is an autoimmune disease characterized by damage to multiple systems and a higher risk of cardiovascular disease. In addition, several studies have found that insulin resistance (IR) is more prevalent in SLE patients than controls, increasing the risk of prediabetes, type 2 diabetes mellitus (T2DM) and morbidity. The objective of this review article was to summarize the most relevant evidence about the relationship among IR, T2DM and SLE, including the effects of proinflammatory states, acute-phase proteins, pro-inflammatory cytokines, and pharmacological SLE treatment. A better understanding of the mechanisms involved in these comorbidities will allow better treatment strategies.
Keywords: Systemic lupus erythematosus, insulin resistance, diabetes mellitus, T2DM, autoimmune disease, prediabetes.
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Graphical Abstract

[1]
Dörner, T.; Furie, R. Novel paradigms in systemic lupus erythematosus. Lancet,  2019, 393(10188), 2344-2358.
 [http://dx.doi.org/10.1016/S0140-6736(19)30546-X] [PMID:  31180031]

[2]
Yurkovich, M.; Vostretsova, K.; Chen, W.; Aviña-Zubieta, J.A. Overall and cause-specific mortality in patients with systemic lupus erythematosus: A meta-analysis of observational studies. Arthritis Care Res. (Hoboken),  2014, 66(4), 608-616.
 [http://dx.doi.org/10.1002/acr.22173] [PMID:  24106157]

[3]
Ormazabal, V.; Nair, S.; Elfeky, O.; Aguayo, C.; Salomon, C.; Zuñiga, F.A. Association between insulin resistance and the development of cardiovascular disease. Cardiovasc. Diabetol.,  2018, 17(1), 122.
 [http://dx.doi.org/10.1186/s12933-018-0762-4] [PMID:  30170598]

[4]
Lebovitz, H. Insulin resistance: Definition and consequences. Exp. Clin. Endocrinol. Diabetes,  2001, 109(Suppl. 2), S135-S148.
 [http://dx.doi.org/10.1055/s-2001-18576] [PMID:  11460565]

[5]
American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care,  2012, 35(Suppl. 1), S64-S71.
 [http://dx.doi.org/10.2337/dc12-s064] [PMID:  22187472]

[6]
Escárcega, R.O.; García-Carrasco, M.; Fuentes-Alexandro, S.; Jara, L.J.; Rojas-Rodriguez, J.; Escobar-Linares, L.E.; Cervera, R. Insulin resistance, chronic inflammatory state and the link with systemic lupus erythematosus-related coronary disease. Autoimmun. Rev.,  2006, 6(1), 48-53.
 [http://dx.doi.org/10.1016/j.autrev.2006.07.001] [PMID:  17110317]

[7]
Mok, C.C. Metabolic syndrome and systemic lupus erythematosus: The connection. Expert Rev. Clin. Immunol.,  2019, 15(7), 765-775.
 [http://dx.doi.org/10.1080/1744666X.2019.1620601] [PMID:  31094570]

[8]
Miyake, C.N.H.; Gualano, B.; Dantas, W.S.; Pereira, R.T.; Neves, W.; Zambelli, V.O.; Shinjo, S.K.; Pereira, R.M.; Silva, E.R.; Sá-Pinto, A.L.; Borba, E.; Roschel, H.; Bonfá, E.; Benatti, F.B. Increased insulin resistance and glucagon levels in mild/inactive systemic lupus erythematosus patients despite normal glucose tolerance. Arthritis Care Res. (Hoboken),  2018, 70(1), 114-124.
 [http://dx.doi.org/10.1002/acr.23237] [PMID:  28320046]

[9]
Chung, C.P.; Oeser, A.; Solus, J.F.; Gebretsadik, T.; Shintani, A.; Avalos, I.; Sokka, T.; Raggi, P.; Pincus, T.; Stein, C.M. Inflammation‐associated insulin resistance: Differential effects in rheumatoid arthritis and systemic lupus erythematosus define potential mechanisms. Arthritis Rheum.,  2008, 58(7), 2105-2112.
 [http://dx.doi.org/10.1002/art.23600] [PMID:  18576352]

[10]
Sabio, J.M.; Vargas-Hitos, J.; Zamora-Pasadas, M.; Mediavilla, J.D.; Navarrete, N.; Ramirez, Á.; Hidalgo-Tenorio, C.; Jáimez, L.; Martín, J.; Jiménez-Alonso, J. Metabolic syndrome is associated with increased arterial stiffness and biomarkers of subclinical atherosclerosis in patients with systemic lupus erythematosus. J. Rheumatol.,  2009, 36(10), 2204-2211.
 [http://dx.doi.org/10.3899/jrheum.081253] [PMID:  19723903]

[11]
Czech, M.P. Insulin action and resistance in obesity and type 2 diabetes. Nat. Med.,  2017, 23(7), 804-814.
 [http://dx.doi.org/10.1038/nm.4350] [PMID:  28697184]

[12]
Sesti, G. Pathophysiology of insulin resistance. Best Pract. Res. Clin. Endocrinol. Metab.,  2006, 20(4), 665-679.
 [http://dx.doi.org/10.1016/j.beem.2006.09.007] [PMID:  17161338]

[13]
DeFronzo, R.A.; Ferrannini, E.; Groop, L.; Henry, R.R.; Herman, W.H.; Holst, J.J.; Hu, F.B.; Kahn, C.R.; Raz, I.; Shulman, G.I.; Simonson, D.C.; Testa, M.A.; Weiss, R. Type 2 diabetes mellitus. Nat. Rev. Dis. Primers,  2015, 1(1), 15019.
 [http://dx.doi.org/10.1038/nrdp.2015.19] [PMID:  27189025]

[14]
Contreras-Haro, B.; Hernandez-Gonzalez, S.O.; Gonzalez-Lopez, L.; Espinel-Bermudez, M.C.; Garcia-Benavides, L.; Perez-Guerrero, E.; Vazquez-Villegas, M.L.; Robles-Cervantes, J.A.; Salazar-Paramo, M.; Hernandez-Corona, D.M.; Nava-Zavala, A.H.; Gamez-Nava, J.I. Fasting triglycerides and glucose index: A useful screening test for assessing insulin resistance in patients diagnosed with rheumatoid arthritis and systemic lupus erythematosus. Diabetol. Metab. Syndr.,  2019, 11(1), 95.
 [http://dx.doi.org/10.1186/s13098-019-0495-x] [PMID:  31788032]

[15]
Ryan, M.J.; McLemore, G.R., Jr; Hendrix, S.T. Insulin resistance and obesity in a mouse model of systemic lupus erythematosus. Hypertension,  2006, 48(5), 988-993.
 [http://dx.doi.org/10.1161/01.HYP.0000243612.02929.df] [PMID:  16982954]

[16]
Gabriel, C.L.; Smith, P.B.; Mendez-Fernandez, Y.V.; Wilhelm, A.J.; Ye, A.M.; Major, A.S. Autoimmune-mediated glucose intolerance in a mouse model of systemic lupus erythematosus. Am. J. Physiol. Endocrinol. Metab.,  2012, 303(11), E1313-E1324.
 [http://dx.doi.org/10.1152/ajpendo.00665.2011] [PMID:  23032686]

[17]
Sada, K.E.; Yamasaki, Y.; Maruyama, M.; Sugiyama, H.; Yamamura, M.; Maeshima, Y.; Makino, H. Altered levels of adipocytokines in association with insulin resistance in patients with systemic lupus erythematosus. J. Rheumatol.,  2006, 33(8), 1545-1552.
 [PMID:  16881111]

[18]
Kuo, C.Y.; Tsai, T.Y.; Huang, Y.C. Insulin resistance and serum levels of adipokines in patients with systemic lupus erythematosus: A systematic review and meta-analysis. Lupus,  2020, 29(9), 1078-1084.
 [http://dx.doi.org/10.1177/0961203320935185] [PMID:  32605528]

[19]
Gigante, A.; Iannazzo, F.; Navarini, L.; Sgariglia, M.C.; Margiotta, D.P.E.; Vaiarello, V.; Foti, F.; Afeltra, A.; Cianci, R.; Rosato, E. Metabolic syndrome and adipokine levels in systemic lupus erythematosus and systemic sclerosis. Clin. Rheumatol.,  2021, 40(10), 4253-4258.
 [http://dx.doi.org/10.1007/s10067-021-05731-6] [PMID:  33839992]

[20]
Senn, J.J.; Klover, P.J.; Nowak, I.A.; Mooney, R.A. Interleukin-6 induces cellular insulin resistance in hepatocytes. Diabetes,  2002, 51(12), 3391-3399.
 [http://dx.doi.org/10.2337/diabetes.51.12.3391] [PMID:  12453891]

[21]
Wang, X.; Bao, W.; Liu, J.; OuYang, Y.Y.; Wang, D.; Rong, S.; Xiao, X.; Shan, Z.L.; Zhang, Y.; Yao, P.; Liu, L.G. Inflammatory markers and risk of type 2 diabetes: A systematic review and meta-analysis. Diabetes Care,  2013, 36(1), 166-175.
 [http://dx.doi.org/10.2337/dc12-0702] [PMID:  23264288]

[22]
Tso, T.K.; Huang, W.N.; Huang, H.Y.; Chang, C.K. Relationship of plasma interleukin-18 concentrations to traditional and non-traditional cardiovascular risk factors in patients with systemic lupus erythematosus. Rheumatology (Oxford),  2006, 45(9), 1148-1153.
 [http://dx.doi.org/10.1093/rheumatology/kel082] [PMID:  16527878]

[23]
Tso, T.K.; Huang, W.N. Elevated soluble intercellular adhesion molecule-1 levels in patients with systemic lupus erythematosus: Relation to insulin resistance. J. Rheumatol.,  2007, 34(4), 726-730.
 [PMID:  17309130]

[24]
Miwa, I.; Ichimura, N.; Sugiura, M.; Hamada, Y.; Taniguchi, S. Inhibition of glucose-induced insulin secretion by 4-hydroxy-2-nonenal and other lipid peroxidation products. Endocrinology,  2000, 141(8), 2767-2772.
 [http://dx.doi.org/10.1210/endo.141.8.7614] [PMID:  10919261]

[25]
Lozovoy, M.A.B.; Simão, A.N.C.; Oliveira, S.R.; Iryioda, T.M.V.; Panis, C.; Cecchini, R.; Dichi, I. Relationship between iron metabolism, oxidative stress, and insulin resistance in patients with systemic lupus erythematosus. Scand. J. Rheumatol.,  2013, 42(4), 303-310.
 [http://dx.doi.org/10.3109/03009742.2012.754942] [PMID:  23424997]

[26]
Koca, S.S.; Karaca, I.; Yavuzkir, M.F.; Dağli, N.; Özgen, M.; Ustündağ, B.; Işik, A. Insulin resistance is related with oxidative stress in systemic lupus erythematosus. Anadolu Kardiyol. Derg.,  2009, 9(1), 23-28.
 [PMID:  19196569]

[27]
Paz, K.; Hemi, R.; LeRoith, D.; Karasik, A.; Elhanany, E.; Kanety, H.; Zick, Y. A molecular basis for insulin resistance. Elevated serine/threonine phosphorylation of IRS-1 and IRS-2 inhibits their binding to the juxtamembrane region of the insulin receptor and impairs their ability to undergo insulin-induced tyrosine phosphorylation. J. Biol. Chem.,  1997, 272(47), 29911-29918.
 [http://dx.doi.org/10.1074/jbc.272.47.29911] [PMID:  9368067]

[28]
Evans, J.L.; Goldfine, I.D.; Maddux, B.A.; Grodsky, G.M. Oxidative stress and stress-activated signaling pathways: A unifying hypothesis of type 2 diabetes. Endocr. Rev.,  2002, 23(5), 599-622.
 [http://dx.doi.org/10.1210/er.2001-0039] [PMID:  12372842]

[29]
DeFronzo, R.A.; Tobin, J.D.; Andres, R. Glucose clamp technique: A method for quantifying insulin secretion and resistance. Am. J. Physiol.,  1979, 237(3), E214-E223.
 [PMID:  382871]

[30]
Muniyappa, R.; Lee, S.; Chen, H.; Quon, M.J. Current approaches for assessing insulin sensitivity and resistance in vivo: Advantages, limitations, and appropriate usage. Am. J. Physiol. Endocrinol. Metab.,  2008, 294(1), E15-E26.
 [http://dx.doi.org/10.1152/ajpendo.00645.2007] [PMID:  17957034]

[31]
Matthews, D.R.; Hosker, J.P.; Rudenski, A.S.; Naylor, B.A.; Treacher, D.F.; Turner, R.C. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia,  1985, 28(7), 412-419.
 [http://dx.doi.org/10.1007/BF00280883] [PMID:  3899825]

[32]
Katz, A.; Nambi, S.S.; Mather, K.; Baron, A.D.; Follmann, D.A.; Sullivan, G.; Quon, M.J. Quantitative insulin sensitivity check index: A simple, accurate method for assessing insulin sensitivity in humans. J. Clin. Endocrinol. Metab.,  2000, 85(7), 2402-2410.
 [http://dx.doi.org/10.1210/jcem.85.7.6661] [PMID:  10902785]

[33]
Matsuda, M.; DeFronzo, R.A. Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp. Diabetes Care,  1999, 22(9), 1462-1470.
 [http://dx.doi.org/10.2337/diacare.22.9.1462] [PMID:  10480510]

[34]
Cobb, J.; Gall, W.; Adam, K.P.; Nakhle, P.; Button, E.; Hathorn, J.; Lawton, K.; Milburn, M.; Perichon, R.; Mitchell, M.; Natali, A.; Ferrannini, E. A novel fasting blood test for insulin resistance and prediabetes. J. Diabetes Sci. Technol.,  2013, 7(1), 100-110.
 [http://dx.doi.org/10.1177/193229681300700112] [PMID:  23439165]

[35]
Tso, T.K.; Huang, H.Y.; Chang, C.K.; Liao, Y.J.; Huang, W.N. Clinical evaluation of insulin resistance and beta-cell function by the homeostasis model assessment in patients with systemic lupus erythematosus. Clin. Rheumatol.,  2004, 23(5), 416-420.
 [http://dx.doi.org/10.1007/s10067-004-0908-5] [PMID:  15459813]

[36]
Mok, C.C.; Tse, S.M.; Chan, K.L.; Ho, L.Y. Effect of the metabolic syndrome on organ damage and mortality in patients with systemic lupus erythematosus: A longitudinal analysis. Clin. Exp. Rheumatol.,  2018, 36(3), 389-395.
 [PMID:  29148424]

[37]
Mobini, M.; Niksolat, F.; Mohammadpour, R.A.; Dashti Dargahloo, S.; Marzban, D. Metabolic syndrome in patients with systemic lupus erythematosus: Association with disease activity, disease damage and age. Int. J. Rheum. Dis.,  2018, 21(5), 1023-1030.
 [http://dx.doi.org/10.1111/1756-185X.13276] [PMID:  29611288]

[38]
Mendoza-Pinto, C.; García-Carrasco, M.; Díaz-Merino, G.; Soto-Santillan, P.; Mejia-Ocampo, R.; Munguía-Realpozo, P.; Ruiz-Arguelles, A. Metabolomics analysis of insulin resistance in mild/inactive non-diabetic systemic lupus erythematosus women. Arthritis Rheumatol.,  2018, 70(10), 1-4.

[39]
Santos, M.J.; Vinagre, F.; Silva, J.J.; Gil, V.; Fonseca, J.E. Cardiovascular risk profile in systemic lupus erythematosus and rheumatoid arthritis: A comparative study of female patients. Acta Reumatol. Port.,  2010, 35(3), 325-332.
 [PMID:  20975635]

[40]
Quevedo-Abeledo, J.C.; Sánchez-Pérez, H.; Tejera-Segura, B.; de Armas-Rillo, L.; Ojeda, S.; Erausquin, C.; González-Gay, M.Á.; Ferraz-Amaro, I. Higher prevalence and degree of insulin resistance in patients with rheumatoid arthritis than in patients with systemic lupus erythematosus. J. Rheumatol.,  2021, 48(3), 339-347.
 [http://dx.doi.org/10.3899/jrheum.200435] [PMID:  32541071]

[41]
Sabio, J.M.; Vargas-Hitos, J.A.; Martinez-Bordonado, J.; Navarrete-Navarrete, N.; Díaz-Chamorro, A.; Olvera-Porcel, C.; Zamora, M.; Jiménez-Alonso, J. Association between low 25-hydroxyvitamin D, insulin resistance and arterial stiffness in nondiabetic women with systemic lupus erythematosus. Lupus,  2015, 24(2), 155-163.
 [http://dx.doi.org/10.1177/0961203314551811] [PMID:  25216653]

[42]
Chew, C.; Reynolds, J.A.; Lertratanakul, A.; Wu, P.; Urowitz, M.; Gladman, D.D.; Fortin, P.R.; Bae, S.C.; Gordon, C.; Clarke, A.E.; Bernatsky, S.; Hanly, J.G.; Isenberg, D.; Rahman, A.; Sanchez-Guerrero, J.; Romero-Diaz, J.; Merrill, J.; Wallace, D.; Ginzler, E.; Khamashta, M.; Nived, O.; Jönsen, A.; Steinsson, K.; Manzi, S.; Kalunian, K.; Dooley, M.A.; Petri, M.; Aranow, C.; van Vollenhoven, R.; Stoll, T.; Alarcón, G.S.; Lim, S.S.; Ruiz-Irastorza, G.; Peschken, C.A.; Askanase, A.D.; Kamen, D.L.; İnanç, M.; Ramsey-Goldman, R.; Bruce, I.N. Lower vitamin D is associated with metabolic syndrome and insulin resistance in systemic lupus: Data from an international inception cohort. Rheumatology (Oxford),  2021, 60(10), 4737-4747.
 [http://dx.doi.org/10.1093/rheumatology/keab090] [PMID:  33555325]

[43]
Sato, H.; Miida, T.; Wada, Y.; Maruyama, M.; Murakami, S.; Hasegawa, H.; Kuroda, T.; Narita, I.; Nakano, M.; Gejyo, F. Atherosclerosis is accelerated in patients with long-term well-controlled Systemic Lupus Erythematosus (SLE). Clin. Chim. Acta,  2007, 385(1-2), 35-42.
 [http://dx.doi.org/10.1016/j.cca.2007.04.023] [PMID:  17644082]

[44]
Liu, S-Y.; Han, L-S.; Guo, J-Y.; Zheng, Z-H.; Li, H.; Zhang, L.; Zhang, X.; He, Y-J.; Gao, G-M.; Liu, Z-S.; Zeng, X-F. Metabolic syndrome in Chinese patients with systemic lupus erythematosus: No association with plasma cortisol level. Lupus,  2013, 22(5), 519-526.
 [http://dx.doi.org/10.1177/0961203313478301] [PMID:  23554041]

[45]
Svenungsson, E.; Fei, G-Z.; Jensen-Urstad, K.; de Faire, U.; Hamsten, A.; Frostegård, J. TNF-α: A link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease. Lupus,  2003, 12(6), 454-461.
 [http://dx.doi.org/10.1191/0961203303lu412oa] [PMID:  12873047]

[46]
Gheita, T.A.; Raafat, H.A.; Sayed, S.; El-Fishawy, H.; Nasrallah, M.M.; Abdel-Rasheed, E. Metabolic syndrome and insulin resistance comorbidity in systemic lupus erythematosus. Z. Rheumatol.,  2013, 72(2), 172-177.
 [http://dx.doi.org/10.1007/s00393-012-1058-9] [PMID:  22990375]

[47]
Sánchez-Pérez, H.; Tejera-Segura, B.; de Vera-González, A.; González-Delgado, A.; Olmos, J.M.; Hernández, J.L.; Corrales, A.; López-Mejías, R.; González-Gay, M.Á.; Ferraz-Amaro, I. Insulin resistance in systemic lupus erythematosus patients: Contributing factors and relationship with subclinical atherosclerosis. Clin. Exp. Rheumatol.,  2017, 35(6), 885-892.
 [PMID:  28281456]

[48]
Goff, D.C., Jr; Lloyd-Jones, D.M.; Bennett, G.; Coady, S.; D’Agostino, R.B.; Gibbons, R.; Greenland, P.; Lackland, D.T.; Levy, D.; O’Donnell, C.J.; Robinson, J.G.; Schwartz, J.S.; Shero, S.T.; Smith, S.C., Jr; Sorlie, P.; Stone, N.J.; Wilson, P.W.F.; Jordan, H.S.; Nevo, L.; Wnek, J.; Anderson, J.L.; Halperin, J.L.; Albert, N.M.; Bozkurt, B.; Brindis, R.G.; Curtis, L.H.; DeMets, D.; Hochman, J.S.; Kovacs, R.J.; Ohman, E.M.; Pressler, S.J.; Sellke, F.W.; Shen, W.K.; Smith, S.C., Jr; Tomaselli, G.F. American College of Cardiology/American Heart Association Task Force on Practice Guidelines 2013 ACC/AHA Guideline on the Assessment of Cardiovascular Risk. Circulation,  2014, 129(25)(Suppl. 2), S49-S73.
 [http://dx.doi.org/10.1161/01.cir.0000437741.48606.98] [PMID:  24222018]

[49]
Arnett, D.K.; Blumenthal, R.S.; Albert, M.A.; Buroker, A.B.; Goldberger, Z.D.; Hahn, E.J.; Himmelfarb, C.D.; Khera, A.; Lloyd-Jones, D.; McEvoy, J.W.; Michos, E.D.; Miedema, M.D.; Muñoz, D.; Smith, S.C., Jr; Virani, S.S.; Williams, K.A., Sr; Yeboah, J.; Ziaeian, B. 2019 ACC/AHA Guideline on the primary prevention of cardiovascular disease: Executive summary. J. Am. Coll. Cardiol.,  2019, 74(10), 1376-1414.
 [http://dx.doi.org/10.1016/j.jacc.2019.03.009] [PMID:  30894319]

[50]
Yu, H.H.; Chen, P.C.; Yang, Y.H.; Wang, L.C.; Lee, J.H.; Lin, Y.T.; Chiang, B.L. Statin reduces mortality and morbidity in systemic lupus erythematosus patients with hyperlipidemia: A nationwide population-based cohort study. Atherosclerosis,  2015, 243(1), 11-18.
 [http://dx.doi.org/10.1016/j.atherosclerosis.2015.08.030] [PMID:  26342937]

[51]
Buse, J.B.; Ginsberg, H.N.; Bakris, G.L.; Clark, N.G.; Costa, F.; Eckel, R.; Fonseca, V.; Gerstein, H.C.; Grundy, S.; Nesto, R.W.; Pignone, M.P.; Plutzky, J.; Porte, D.; Redberg, R.; Stitzel, K.F.; Stone, N.J. Primary prevention of cardiovascular diseases in people with diabetes mellitus: A scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care,  2007, 30(1), 162-172.
 [http://dx.doi.org/10.2337/dc07-9917] [PMID:  17192355]

[52]
Munguia-Realpozo, P.; Mendoza-Pinto, C.; Sierra Benito, C.; Escarcega, R.O.; Garcia-Carrasco, M.; Mendez Martinez, S.; Etchegaray Morales, I.; Galvez Romero, J.L.; Ruiz-Arguelles, A.; Cervera, R. Systemic lupus erythematosus and hypertension. Autoimmun. Rev.,  2019, 18(10), 102371.
 [http://dx.doi.org/10.1016/j.autrev.2019.102371] [PMID:  31415907]

[53]
Heshin-Bekenstein, M.; Trupin, L.; Yelin, E.; von Scheven, E.; Yazdany, J.; Lawson, E.F. Longitudinal disease- and steroid-related damage among adults with childhood-onset systemic lupus erythematosus. Semin. Arthritis Rheum.,  2019, 49(2), 267-272.
 [http://dx.doi.org/10.1016/j.semarthrit.2019.05.010] [PMID:  31235075]

[54]
Monção, C.S.A.; Martins, L.N.; Penteado, M.P.S.; Reis, R.C.P.; Santos, F.M.M.; Lanna, C.C.D.; Ribeiro, A.L.; Telles, R.W. Incidence of cardiovascular risk factors in female patients with systemic lupus erythematosus: A 3-year follow-up cohort. Lupus,  2018, 27(11), 1790-1798.
 [http://dx.doi.org/10.1177/0961203318790676] [PMID:  30099941]

[55]
Jiang, M.Y.; Hwang, J.C.; Feng, I.J. Impact of diabetes mellitus on the risk of end-stage renal disease in patients with systemic lupus erythematosus. Sci. Rep.,  2018, 8(1), 6008.
 [http://dx.doi.org/10.1038/s41598-018-24529-2] [PMID:  29662119]

[56]
Dong, Y.; Dai, Z.; Wang, Z.; Wang, H.; Yuan, F.; Zhu, Y.; Ye, D.; Wang, B. Risk of gestational diabetes mellitus in systemic lupus erythematosus pregnancy: A systematic review and meta-analysis. BMC Pregnancy Childbirth,  2019, 19(1), 179.
 [http://dx.doi.org/10.1186/s12884-019-2329-0] [PMID:  31113392]

[57]
Gernaat, S.A.M.; Simard, J.F.; Wikström, A.K.; Svenungsson, E.; Arkema, E.V. Gestational diabetes mellitus risk in pregnant women with systemic lupus erythematosus. J. Rheumatol.,  2022, 49(5), 465-469.
 [http://dx.doi.org/10.3899/jrheum.210087] [PMID:  34853085]

[58]
Dima, A.; Jurcut, C.; Chasset, F.; Felten, R.; Arnaud, L. Hydroxychloroquine in systemic lupus erythematosus: Overview of current knowledge. Ther. Adv. Musculoskelet. Dis.,  2022, 14, 1759720X211073001.

[59]
Gerstein, H.C.; Thorpe, K.E.; Wayne Taylor, D.; Brian Haynes, R. The effectiveness of hydroxychloroquine in patients with type 2 diabetes mellitus who are refractory to sulfonylureas-a randomized trial. Diabetes Res. Clin. Pract.,  2002, 55(3), 209-219.
 [http://dx.doi.org/10.1016/S0168-8227(01)00325-4] [PMID:  11850097]

[60]
Rekedal, L.; Massarotti, E.; Garg, R.; Bhatia, R.; Gleeson, T.; Lu, B.; Solomon, D. Changes in glycated hemoglobin after initiation of hydroxychloroquine or methotrexate in diabetic patients with rheumatologic diseases. Arthritis Rheum.,  2010, 130(6), 3569-3573.
 [http://dx.doi.org/10.1002/art.27703] [PMID:  20722019]

[61]
Munguía-Realpozo, P.; Mendoza-Pinto, C.; García-Carrasco, M.; Berra-Romani, R.; Sierra-Benito, C.; Méndez-Martínez, S.; Cervera, R. The impact of antimalarial agents on traditional and non-traditional subclinical atherosclerosis biomarkers in systemic lupus erythematosus: A systematic review and meta-analysis. Autoimmun. Rev.,  2021, 20(9), 102887.
 [http://dx.doi.org/10.1016/j.autrev.2021.102887] [PMID:  34237422]

[62]
Chen, Y.M.; Lin, C.H.; Lan, T.H.; Chen, H.H.; Chang, S.N.; Chen, Y.H.; Wang, J.S.; Hung, W.T.; Lan, J.L.; Chen, D.Y. Hydroxychloroquine reduces risk of incident diabetes mellitus in lupus patients in a dose-dependent manner: A population-based cohort study. Rheumatology (Oxford),  2015, 54(7), 1244-1249.
 [http://dx.doi.org/10.1093/rheumatology/keu451] [PMID:  25587177]

[63]
Salmasi, S.; Sayre, E.C.; Antonio Aviña-Zubieta, J.; Esdaile, J.M.; De Vera, M.A. Adherence to antimalarial therapy and risk of type 2 diabetes mellitus among patients with systemic lupus erythematosus: A population‐based study. Arthritis Care Res. (Hoboken),  2021, 73(5), 702-706.
 [http://dx.doi.org/10.1002/acr.24147] [PMID:  31961497]

[64]
Ha, Y.J.; Lee, K-H.; Jung, S.J.; Lee, S-W.; Lee, S-K.; Park, Y-B. Glucocorticoid-induced diabetes mellitus in patients with systemic lupus erythematosus treated with high-dose glucocorticoid therapy. Lupus,  2011, 20(10), 1027-1034.
 [http://dx.doi.org/10.1177/0961203311402246] [PMID:  21659423]

[65]
Zabihi Yeganeh, M.; Sadeghi, S. Risk factors of glucocorticoid-induced diabetes mellitus in systemic lupus erythematosus. Galen Med. J.,  2013, 2(2), 39-43.
 [http://dx.doi.org/10.31661/gmj.v2i2.51]

[66]
El Magadmi, M.; Ahmad, Y.; Turkie, W.; Yates, A.P.; Sheikh, N.; Bernstein, R.M.; Durrington, P.N.; Laing, I.; Bruce, I.N. Hyperinsulinemia, insulin resistance, and circulating oxidized low density lipoprotein in women with systemic lupus erythematosus. J. Rheumatol.,  2006, 33(1), 50-56.
 [PMID:  16395749]

[67]
García-Dorta, A.; Quevedo-Abeledo, J.C.; Rua-Figueroa, Í.; de Vera-González, A.M.; González-Delgado, A.; Medina-Vega, L.; González-Rivero, A.F.; Francisco-Hernández, F.; González-Gay, M.A.; Ferraz-Amaro, I. Beta-cell function is disrupted in patients with systemic lupus erythematosus. Rheumatology (Oxford),  2021, 60(8), 3826-3833.
 [http://dx.doi.org/10.1093/rheumatology/keaa874] [PMID:  33369681]

[68]
Casey, K.A.; Smith, M.A.; Sinibaldi, D.; Seto, N.L.; Playford, M.P.; Wang, X.; Carlucci, P.M.; Wang, L.; Illei, G.; Yu, B.; Wang, S.; Remaley, A.T.; Mehta, N.N.; Kaplan, M.J.; White, W.I. Modulation of cardiometabolic disease markers by type I interferon inhibition in systemic lupus erythematosus. Arthritis Rheumatol.,  2021, 73(3), 459-471.
 [http://dx.doi.org/10.1002/art.41518] [PMID:  32909675]

[69]
Alunno, A.; Carubbi, F.; Bartoloni, E.; Grassi, D.; Ferri, C.; Gerli, R. Diet in rheumatoid arthritis versus systemic lupus erythematosus: Any differences? Nutrients,  2021, 13(3), 772.
 [http://dx.doi.org/10.3390/nu13030772] [PMID:  33673487]

[70]
Pocovi-Gerardino, G.; Correa-Rodríguez, M.; Callejas-Rubio, J.L.; Ríos-Fernández, R.; Martín-Amada, M.; Cruz-Caparros, M.G.; Rueda-Medina, B.; Ortego-Centeno, N. Beneficial effect of Mediterranean diet on disease activity and cardiovascular risk in systemic lupus erythematosus patients: A cross-sectional study. Rheumatology (Oxford),  2021, 60(1), 160-169.
 [http://dx.doi.org/10.1093/rheumatology/keaa210] [PMID:  32594173]

[71]
Terrell, M.; Morel, L. The intersection of cellular and systemic metabolism: Metabolic syndrome in systemic lupus erythematosus. Endocrinology,  2022, 163(7), bqac067.
 [http://dx.doi.org/10.1210/endocr/bqac067] [PMID:  35560001]

[72]
Gorczyca, D.; Szponar, B.; Paściak, M.; Czajkowska, A.; Szmyrka, M. Serum levels of n-3 and n-6 polyunsaturated fatty acids in patients with systemic lupus erythematosus and their association with disease activity: A pilot study. Scand. J. Rheumatol.,  2022, 51(3), 230-236.
 [http://dx.doi.org/10.1080/03009742.2021.1923183] [PMID:  34169789]

[73]
Hahn, J.; Cook, N.R.; Alexander, E.K.; Friedman, S.; Walter, J.; Bubes, V.; Kotler, G.; Lee, I.M.; Manson, J.E.; Costenbader, K.H. Vitamin D and marine omega 3 fatty acid supplementation and incident autoimmune disease: VITAL randomized controlled trial. BMJ,  2022, 376, e066452.
 [http://dx.doi.org/10.1136/bmj-2021-066452] [PMID:  35082139]

[74]
Fisher, S.A.; Rahimzadeh, M.; Brierley, C.; Gration, B.; Doree, C.; Kimber, C.E.; Plaza Cajide, A.; Lamikanra, A.A.; Roberts, D.J. The role of vitamin D in increasing circulating T regulatory cell numbers and modulating T regulatory cell phenotypes in patients with inflammatory disease or in healthy volunteers: A systematic review. PLoS One,  2019, 14(9), e0222313.
 [http://dx.doi.org/10.1371/journal.pone.0222313] [PMID:  31550254]

[75]
Rajaei, E.; Mowla, K.; Ghorbani, A.; Bahadoram, S.; Bahadoram, M.; Dargahi-Malamir, M. The effect of omega-3 fatty acids in patients with active rheumatoid arthritis receiving DMARDs therapy: Double-blind randomized controlled trial. Glob. J. Health Sci.,  2015, 8(7), 18-25.
 [http://dx.doi.org/10.5539/gjhs.v8n7p18] [PMID:  26925896]

[76]
Schäfer, A.L.; Eichhorst, A.; Hentze, C.; Kraemer, A.N.; Amend, A.; Sprenger, D.T.L.; Fluhr, C.; Finzel, S.; Daniel, C.; Salzer, U.; Rizzi, M.; Voll, R.E.; Chevalier, N. Low dietary fiber intake links development of obesity and lupus pathogenesis. Front. Immunol.,  2021, 12, 696810.
 [http://dx.doi.org/10.3389/fimmu.2021.696810] [PMID:  34335609]

[77]
Akbar, U.; Yang, M.; Kurian, D.; Mohan, C. Omega-3 fatty acids in rheumatic diseases. J. Clin. Rheumatol.,  2017, 23(6), 330-339.
 [http://dx.doi.org/10.1097/RHU.0000000000000563] [PMID:  28816722]

[78]
Pedro, E.M.; da Rosa Franchi Santos, L.F.; Scavuzzi, B.M.; Iriyoda, T.M.V.; Peixe, T.S.; Lozovoy, M.A.B.; Reiche, E.M.V.; Dichi, I.; Simão, A.N.C.; Santos, M.J. Trace elements associated with systemic lupus erythematosus and insulin resistance. Biol. Trace Elem. Res.,  2019, 191(1), 34-44.
 [http://dx.doi.org/10.1007/s12011-018-1592-7] [PMID:  30600500]

[79]
do Prado, R.; Aires, P.P.; Suano-Souza, F.I.; Affonso Fonseca, F.L.; Terreri, M.T.; Sarni, R.O.S. Selenium nutritional status and its association with SLEDAI-2K, HOMA-IR and lipid profile in Juvenile Systemic Lupus Erythematosus patients. Lupus,  2022, 31(2), 155-162.
 [http://dx.doi.org/10.1177/09612033211067982] [PMID:  35077255]

[80]
Islam, M.A.; Khandker, S.S.; Kotyla, P.J.; Hassan, R. Immunomodulatory effects of diet and nutrients in Systemic Lupus Erythematosus (SLE): A systematic review. Front. Immunol.,  2020, 11, 1477.
 [http://dx.doi.org/10.3389/fimmu.2020.01477] [PMID:  32793202]

[81]
Frostegård, J. Prediction and management of cardiovascular outcomes in systemic lupus erythematosus. Expert Rev. Clin. Immunol.,  2015, 11(2), 247-253.
 [http://dx.doi.org/10.1586/1744666X.2015.993970] [PMID:  25517760]

[82]
Davies, R.J.; Lomer, M.C.E.; Yeo, S.I.; Avloniti, K.; Sangle, S.R.; D’Cruz, D.P. Weight loss and improvements in fatigue in systemic lupus erythematosus: A controlled trial of a low glycaemic index diet versus a calorie restricted diet in patients treated with corticosteroids. Lupus,  2012, 21(6), 649-655.
 [http://dx.doi.org/10.1177/0961203312436854] [PMID:  22311939]

[83]
Sun, F.; Wang, H.J.; Liu, Z.; Geng, S.; Wang, H.T.; Wang, X.; Li, T.; Morel, L.; Wan, W.; Lu, L.; Teng, X.; Ye, S. Safety and efficacy of metformin in systemic lupus erythematosus: A multicentre, randomised, double-blind, placebo-controlled trial. Lancet Rheumatol.,  2020, 2(4), e210-e216.
 [http://dx.doi.org/10.1016/S2665-9913(20)30004-7]

[84]
Teng, X.; Brown, J.; Morel, L. Redox homeostasis involvement in the pharmacological effects of metformin in systemic lupus erythematosus. Antioxid. Redox Signal.,  2022, 36(7-9), 462-479.
 [http://dx.doi.org/10.1089/ars.2021.0070] [PMID:  34619975]

[85]
Pharmacologic approaches to glycemic treatment: Standards of medical care in diabetes-2022. Diabetes Care,  2022, 45(Suppl. 1), S125-S143.

[86]
Zelniker, T.A.; Wiviott, S.D.; Raz, I. Im, K.; Goodrich, E.L.; Bonaca, M.P.; Mosenzon, O.; Kato, E.T.; Cahn, A.; Furtado, R.H.M.; Bhatt, D.L.; Leiter, L.A.; McGuire, D.K.; Wilding, J.P.H.; Sabatine, M.S. SGLT2 inhibitors for primary and secondary prevention of cardiovascular and renal outcomes in type 2 diabetes: A systematic review and meta-analysis of cardiovascular outcome trials. Lancet,  2019, 393(10166), 31-39.
 [http://dx.doi.org/10.1016/S0140-6736(18)32590-X] [PMID:  30424892]

[87]
Davies, M.J.; D’Alessio, D.A.; Fradkin, J.; Kernan, W.N.; Mathieu, C.; Mingrone, G.; Rossing, P.; Tsapas, A.; Wexler, D.J.; Buse, J.B. Management of Hyperglycemia in Type 2 Diabetes, 2018. A Consensus Report by the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD). Diabetes Care,  2018, 41(12), 2669-2701.
 [http://dx.doi.org/10.2337/dci18-0033] [PMID:  30291106]

[88]
Tso, T.K.; Huang, W.N. Elevation of fasting insulin and its association with cardiovascular disease risk in women with systemic lupus erythematosus. Rheumatol. Int.,  2009, 29(7), 735-742.
 [http://dx.doi.org/10.1007/s00296-008-0781-7] [PMID:  19037607]

[89]
Chung, C.P.; Long, A.G.; Solus, J.F.; Rho, Y.H.; Oeser, A.; Raggi, P.; Stein, C.M. Adipocytokines in systemic lupus erythematosus: Relationship to inflammation, insulin resistance and coronary atherosclerosis. Lupus,  2009, 18(9), 799-806.
 [http://dx.doi.org/10.1177/0961203309103582] [PMID:  19578104]

[90]
Demir, S.; Erten, G.; Artım-Esen, B.; Şahinkaya, Y.; Pehlivan, Ö.; Alpay-Kanıtez, N.; Deniz, G.; Inanç, M. 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(9), 1509-1516.
 [http://dx.doi.org/10.1177/0961203318782424] [PMID:  29954279]

[91]
Baker, J.F.; Morales, M.; Qatanani, M.; Cucchiara, A.; Nackos, E.; Lazar, M.A.; Teff, K.; Von Feldt, J.M. Resistin levels in lupus and associations with disease-specific measures, insulin resistance, and coronary calcification. J. Rheumatol.,  2011, 38(11), 2369-2375.
 [http://dx.doi.org/10.3899/jrheum.110237] [PMID:  21885493]

[92]
Ormseth, M.J.; Swift, L.L.; Fazio, S.; Linton, M.F.; Raggi, P.; Solus, J.F.; Oeser, A.; Bian, A.; Gebretsadik, T.; Shintani, A.; Stein, C.M. Free fatty acids are associated with metabolic syndrome and insulin resistance but not inflammation in systemic lupus erythematosus. Lupus,  2013, 22(1), 26-33.
 [http://dx.doi.org/10.1177/0961203312462756] [PMID:  23060481]

[93]
Shaaban, A.; Helmy, M.; Barakat, M.; Elneily, D.; Ahmed, O. Serum resistin, insulin resistance and carotid intima-media thickness as an indication of subclinical atherosclerosis in systemic lupus erythematosus patients. Egypt. Rheumatol.,  2020, 43(20), 319-323.

[94]
Svenungsson, E.; Jensen-Urstad, K.; Heimbürger, M.; Silveira, A.; Hamsten, A.; de Faire, U.; Witztum, J.L.; Frostegård, J. Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation,  2001, 104(16), 1887-1893.
 [http://dx.doi.org/10.1161/hc4101.097518] [PMID:  11602489]

[95]
Bruce, I.N.; Urowitz, M.B.; Gladman, D.D.; 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(11), 3159-3167.
 [http://dx.doi.org/10.1002/art.11296] [PMID:  14613278]

[96]
Cortes, S.; Chambers, S.; Jerónimo, A.; Isenberg, D. Diabetes mellitus complicating systemic lupus erythematosus - analysis of the UCL lupus cohort and review of the literature. Lupus,  2008, 17(11), 977-980.
 [http://dx.doi.org/10.1177/0961203308091539] [PMID:  18852220]

[97]
Zeng, Y-J.; Zeng, F-Q.; Dai, L.; Yang, C.; Lin, B-Z.; Zheng, D-H.; Liu, D.; Yan, L.; Ren, M.; Cheng, H. Characteristics and risk factors for hyperglycemia in Chinese female patients with systemic lupus erythematosus. Lupus,  2010, 19(11), 1344-1350.
 [http://dx.doi.org/10.1177/0961203310375439] [PMID:  20693192]

[98]
Shaharir, S.S.; Gafor, A.H.A.; Said, M.S.M.; Kong, N.C.T. Steroid-induced diabetes mellitus in systemic lupus erythematosus patients: Analysis from a Malaysian multi-ethnic lupus cohort. Int. J. Rheum. Dis.,  2015, 18(5), 541-547.
 [http://dx.doi.org/10.1111/1756-185X.12474] [PMID:  25294584]
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DOI https://dx.doi.org/10.2174/1871530322666220908154253	Print ISSN 1871-5303
Publisher Name Bentham Science Publisher	Online ISSN 2212-3873
Endocrine, Metabolic & Immune Disorders - Drug Targets

Insulin Resistance and Diabetes Mellitus in Patients with Systemic Lupus Erythematosus

Abstract

Graphical Abstract

Association between Diabetes Mellitus and natural product complementary applications: State of the arts

Chronic inflammation and Disorders/Cancers

Immune defense of the blood-tissue barriers which are related to drugs, metabolic and hormones

Endocrine, Metabolic & Immune Disorders - Drug Targets

Insulin Resistance and Diabetes Mellitus in Patients with Systemic Lupus Erythematosus

Abstract

Graphical Abstract

Call for Papers in Thematic Issues

Association between Diabetes Mellitus and natural product complementary applications: State of the arts

Chronic inflammation and Disorders/Cancers

Immune defense of the blood-tissue barriers which are related to drugs, metabolic and hormones

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