Influence of biologics on carbohydrate metabolism and risk of diabetes
https://doi.org/10.14412/1995-4484-2019-222-228
Abstract
In the article the analysis of the literature on the impact of biologics of different groups (inhibitors of tumor necrosis factor α, tocilizumab, abatacept, rituximab and interleukin 1 inhibitors) on the production of insulin by the pancreas, insulin resistance and the risk of development of the 2nd type diabetes in patients with rheumatic diseases.
About the Authors
L. V. KondratievaRussian Federation
34A, Kashirskoe Shosse, Moscow, 115522
T. V. Popkova
Russian Federation
34A, Kashirskoe Shosse, Moscow, 115522
E. L. Nasonov
Russian Federation
34A, Kashirskoe Shosse, Moscow, 115522;
8, Trubetskaya Str., Build. 2, Moscow, 119991
References
1. Nasonov EL, Karateev DE. Rheumatoid arthritis. In: Nasonov EL, editor. Rossiiskie klinicheskie rekomendatsii. Revmatologiya [Russian clinical recommendations. Rheumatology]. Moscow: GEOTAR-Media; 2017. P. 17-57 (In Russ.).
2. Solomon DH, Massarotti E, Garg R, et al. Association between disease-modifying antirheumatic drugs and diabetes risk in patients with rheumatoid arthritis and psoriasis. JAMA. 2011;305:2525-31. doi: 10.1001/jama.2011.878
3. Antohe J, Bili A, Sartorius JA, et al. Diabetes mellitus risk in rheumatoid arthritis: reduced incidence with anti-tumor necrosis factor αtherapy. Arthritis Care Res. 2012;64(2):215-21. doi: 10.1002/acr.20657
4. Ozen G, Pedro S, Holmqvist ME, et al. Risk of diabetes mellitus associated with disease-modifying antirheumatic drugs and statins in rheumatoid arthritis. Ann Rheum Dis. 2017;76:848-54. doi: 10.1136/annrheumdis-2016-209954
5. Gupta-Ganguli M, Cox K, Means B, et al. Does therapy with antiTNF-γimprove glucose tolerance and control in patients with type 2 diabetes? Diabetes Care. 2011;34:e121. doi: 10.2337/dc10-1334
6. Da Silva BS, Bonfa E, de Moraes JC, et al. Effects of anti-TNF therapy on glucose metabolism in patients with ankylosing spondylitis, psoriatic arthritis or juvenile idiopathic arthritis. Biologicals. 2010;38(5):567-9. doi: 10.1016/j.biologicals.2010.05.003
7. Wood PR, Manning E, Baker JF, et al. Blood glucose changes surrounding initiation of tumor-necrosis factor inhibitors and conventional disease-modifying anti-rheumatic drugs in veterans with rheumatoid arthritis. World J Diabetes. 2018;9(2):53-8. doi: 10.4239/wjd.v9.i2.53
8. Dominguez H, Storgaard H, Rask-Madsen C, et al. Metabolic and Vascular Effects of Tumor Necrosis Factor-αBlockade with Etanercept in Obese Patients with Type 2 Diabetes. J Vasc Res. 2005;42:517-25. doi: 10.1159/000088261
9. Paquot N, Castillo MJ, Lefebvre PJ, Scheen AJ. No increased insulin sensitivity after a single intravenous administration of a recombinant human tumor necrosis factor receptor: Fc fusion protein in obese insulin-resistant patients. J Clin Endocrinol Metab. 2000;85:1316-9. doi: 10.1210/jcem.85.3.6417
10. Di Rocco P, Manco M, Rosa G, et al. Lowered tumor necrosis factor receptors, but not increased insulin sensitivity, with infliximab. Obes Res. 2004;12:734-9. doi: 10.1038/oby.2004.86
11. Miranda-Filloy JA, Llorca J, Carnero-Lopez B, et al. TNF-alpha antagonist therapy improves insulin sensitivity in non-diabetic ankylosing spondylitis patients. Clin Exper Rheumatol. 2012;30:850-5.
12. Gonzalez-Gay MA, De Matias J M, Gonzalez-Juanatey C, et al. Anti-tumor necrosis factor-alpha blockade improves insulin resistance in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2006;24:83-6.
13. Tam LS, Tomlinson B, Chu TT, et al. Impact of TNF inhibition on insulin resistance and lipids levels in patients with rheumatoid arthritis. Clin Rheumatol. 2007;26(9):1495-8. doi: 10.1007/s10067-007-0539-8
14. Oguz FM, Oguz A, Uzunlulu M. The effect of infliximab treatment on insulin resistance in patients with rheumatoid arthritis. Acta Clin Belg. 2007;62(4):218-22. doi: 10.1179/acb.2007.035
15. Seriolo B, Ferrone C, Cutolo M. Longterm anti-tumor necrosis factor-alpha treatment in patients with refractory rheumatoid arthritis: relationship between insulin resistance and disease activity. J Rheumatol. 2008;35(2):355-7.
16. Bissell LA, Hensor EM, Kozera L, et al. Improvement in insulin resistance is greater when infliximab is added to methotrexate during intensive treatment of early rheumatoid arthritis – results from the IDEA study. Rheumatology. 2016;55(12):2181-90. doi: 10.1093/rheumatology/kew306
17. Chen DY, Chen YM, Hsieh TY, et al. Significant effects of biologic therapy on lipid profiles and insulin resistance in patients with rheumatoid arthritis. Arthritis Res Ther. 2015;17:52. doi: 10.1186/s13075-015-0559-8
18. Nam JL, Villeneuve E, Hensor EM, et al. Remission induction comparing infliximab and high-dose intravenous steroid, followed by treat-to-target: a double-blind, randomised, controlled trial in new-onset, treatment-naive, rheumatoid arthritis (the IDEA study). Ann Rheum Dis. 2014;73(1):75-85. doi: 10.1136/annrheumdis-2013-203440
19. Rosenvinge A, Krogh-Madsen R, Baslund B, Pedersen BK. Insulin resistance in patients with rheumatoid arthritis: effect of anti-TNFa therapy. Scand J Rheumatol. 2007;36(2):91-6. doi: 10.1080/03009740601179605
20. Stavropoulos-Kalinoglou A, Metsios GS, Panoulas VF, et al. Antitumour necrosis factor alpha therapy improves insulin sensitivity in normal-weight but not in obese patients with rheumatoid arthritis. Arthritis Res Ther. 2012;14(4):R160. doi: 10.1186/ar3900
21. Kiortsis DN, Mavridis AK, Vasakos S, et al. Effects of infliximab treatment on insulin resistance in patients with rheumatoid arthritis and ankylosing spondylitis. Ann Rheum Dis. 2005;64(5):765-6. doi: 10.1136/ard.2004.026534
22. Stagakis I, Bertsias G, Karvounaris S, et al. Anti-tumor necrosis factor therapy improves insulin resistance, beta cell function and insulin signaling in active rheumatoid arthritis patients with high insulin resistance. Arthritis Res Ther. 2012;14(3):R141. doi: 10.1186/ar3874
23. Ferraz-Amaro I, Arce-Franco M, Muniz J, et al. Systemic blockade of TNF-αdoes not improve insulin resistance in humans. Horm Metab Res. 2011;43(11):801-8. doi: 10.1055/s-0031-1287783
24. Pina T, Armesto S, Lopez-Mejias R, et al. Anti-TNF-αtherapy improves insulin sensitivity in non-diabetic patients with psoriasis: a 6-month prospective study. J Eur Acad Dermatol Venereol. 2015;29(7):1325-30. doi: 10.1111/jdv.12814
25. Marra M, Campanati A, Testa R, et al. Effect of etanercept on insulin sensitivity in nine patients with psoriasis. Int J Immunopathol Pharmacol. 2007;20(4):731-6. doi: 10.1177/039463200702000408
26. Martinez-Abundis E, Reynoso-von Drateln C, Hernandez-Salazar E, Gonzalez-Ortiz M. Effect of etanercept on insulin secretion and insulin sensitivity in a randomized trial with psoriatic patients at risk for developing type 2 diabetes mellitus. Arch Dermatol Res. 2007 Nov;299(9):461-5. doi: 10.1007/s00403-007-0784-3
27. Koutroubakis IE, Oustamanolakis P, Malliaraki N, et al. Effects of tumor necrosis factor alpha inhibition with infliximab on lipid levels and insulin resistance in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2009;21(3):283-8. doi: 10.1097/MEG.0b013e328325d42b
28. Orban T, Bundy B, Becker DJ, et al. Co-stimulation modulation with abatacept in patients with recent-onset type 1 diabetes: a randomised, double-blind, placebo-controlled trial. Lancet. 2011;378(9789):412-9. doi: 10.1016/S0140-6736(11)60886-6
29. Orban T, Bundy B, Becker DJ, et al. Costimulation modulation with abatacept in patients with recent-onset type 1 diabetes: follow-up 1 year after cessation of treatment. Diabetes Care. 2014;37(4):1069-75. doi: 10.2337/dc13-0604
30. Orban T, Beam CA, Xu P, et al. Reduction in CD4 central memory T-cell subset in costimulation modulator abatacept-treated patients with recent-onset type 1 diabetes is associated with slower C-peptide decline. Diabetes. 2014;63(10):3449-57. doi: 10.2337/db14-0047
31. Fujii M, Inoguchi T, Batchuluun B, et al. CTLA-4Ig immunotherapy of obesity-induced insulin resistance by manipulation of macrophage polarization in adipose tissues. Biochem Biophys Res Commun. 2013;438(1):103-9. doi: 10.1016/j.bbrc.2013.07.034
32. Ursini F, Russo E, Letizia Hribal M, et al. Abatacept improves whole-body insulin sensitivity in rheumatoid arthritis: an observational study. Medicine (Baltimore). 2015;94(21):e888. doi: 10.1097/MD.0000000000000888
33. Ogata A, Morishima A, Hirano T, et al. Improvement of HbA1c during treatment with humanised anti-interleukin 6 receptor antibody, tocilizumab. Ann Rheum Dis. 2011;70(6):1164-5. doi: 10.1136/ard.2010.132845
34. Otsuka Y, Kiyohara C, Kashiwado Y,et al. Effects of tumor necrosis factor inhibitors and tocilizumab on the glycosylated hemoglobin levels in patients with rheumatoid arthritis; an observational study. PLoS One. 2018;13(4):e0196368. doi: 10.1371/journal.pone.0196368
35. Schultz O, Oberhauser F, Saech J, et al. Effects of inhibition of interleukin-6 signalling on insulin sensitivity and lipoprotein (a) levels in human subjects with rheumatoid diseases. PLoS One. 2010;5(12):e14328. doi: 10.1371/journal.pone.0014328
36. Mirjafari H, Wang J, Klearman M, et al. Insulin resistance is improved by tocilizumab therapy in rheumatoid arthritis: results from the TOWARD study. Ann Rheum Dis. 2013;72(Suppl 3):A414-5. doi: 10.1136/annrheumdis-2013-eular.1259 [Abstracts book].
37. Makrilakis K, Fragiadaki K, Smith J, et al. Interrelated reduction of chemerin and plasminogen activator inhibitor-1 serum levels in rheumatoid arthritis after interleukin-6 receptor blockade. Clin Rheumatol. 2015 Mar;34(3):419-27. doi: 10.1007/s10067-014-2704-1
38. Tournadre A, Pereira B, Dutheil, et al. Changes in body composition and metabolic profile during interleukin 6 inhibition in rheumatoid arthritis. J Cachexia Sarcopenia Muscle. 2017;8(4):639-46. doi: 10.1002/jcsm.12189
39. Pescovitz MD, Greenbaum CJ, Bundy B, et al. B-lymphocyte depletion with rituximab and β-cell function: two-year results. Diabetes Care. 2014;37(2):453-9. doi: 10.2337/dc13-0626
40. Iseri K, Iyoda M, Shikida Y, et al. Rituximab for the treatment of type B insulin resistance syndrome: a case report and review of the literature. Diabet Med. 2017;34(12):1788-91. doi: 10.1111/dme.13524
41. Klubo-Gwiezdzinska J, Lange M, Cochran E, et al. Combined Immunosuppressive Therapy Induces Remission in Patients With Severe Type B Insulin Resistance: A Prospective Cohort Study. Diabetes Care. 2018;41(11):2353-60. doi: 10.2337/dc18-0884
42. Everett BM, Donath MY, Pradhan AD, et al. Anti-Inflammatory Therapy With Canakinumab for the Prevention and Management of Diabetes. J Am Coll Cardiol. 2018;71(21):2392-401. doi: 10.1016/j.jacc.2018.03.002
43. Ridker PM, Howard CP, Walter V, et al. Effects of interleukin-1β inhibition with canakinumab on hemoglobin A1c, lipids, C-reactive protein, interleukin-6, and fibrinogen: a phase IIb randomized, placebo-controlled trial. Circulation. 2012;126(23):2739-48. doi: 10.1161/CIRCULATIONAHA.112.122556
44. Larsen CM, Faulenbach M, Vaag A, et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med. 2007;356:1517-26. doi: 10.1056/NEJMoa065213
45. Larsen CM, Faulenbach M, Vaag A, et al. Sustained effects of interleukin-1 receptor antagonist treatment in type 2 diabetes. Diabetes Care. 2009;32(9):1663-8. doi: 10.2337/dc09-0533
46. Van Poppel PC, van Asseldonk EJ, Holst JJ, et al. The interleukin-1 receptor antagonist anakinra improves first-phase insulin secretion and insulinogenic index in subjects with impaired glucose tolerance. Diabetes Obes Metab. 2014;16(12):1269-73. doi: 10.1111/dom.12357
47. Moran A, Bundy B, Becker DJ, et al. Interleukin-1 antagonism in type 1 diabetes of recent onset: two multicentre, randomised, double-blind, placebo-controlled trials. Lancet. 2013;381(9881):1905-15. doi: 10.1016/S0140-6736(13)60023-9
48. Rissanen A, Howard CP, Botha J, Thuren T; Global Investigators. Effect of anti-IL-1βantibody (canakinumab) on insulin secretion rates in impaired glucose tolerance or type 2 diabetes: results of a randomized, placebo-controlled trial. Diabetes Obes Metab. 2012;14(12):1088-96. doi: 10.1111/j.1463-1326.2012.01637.x
49. Van Asseldonk EJ, van Poppel PC, Ballak DB, et al. One week treatment with the IL-1 receptor antagonist anakinra leads to a sustained improvement in insulin sensitivity in insulin resistant patients with type 1 diabetes mellitus. Clin Immunol. 2015;160(2):155-62. doi: 10.1016/j.clim.2015.06.003
Review
For citations:
Kondratieva L.V., Popkova T.V., Nasonov E.L. Influence of biologics on carbohydrate metabolism and risk of diabetes. Rheumatology Science and Practice. 2019;57(2):222-228. (In Russ.) https://doi.org/10.14412/1995-4484-2019-222-228