Skip to main content
Top
Published in: Current Diabetes Reports 10/2016

01-10-2016 | Diabetes Epidemiology (N Maruthur, Section Editor)

Immune-Modulating Therapy for Rheumatologic Disease: Implications for Patients with Diabetes

Authors: Scott J. Pilla, Amy Q. Quan, Emily L. Germain-Lee, David B. Hellmann, Nestoras N. Mathioudakis

Published in: Current Diabetes Reports | Issue 10/2016

Login to get access

Abstract

Immune modulators used to treat rheumatologic disease have diverse endocrine effects in patients with diabetes. Providers should be aware of these effects given that diabetes and rheumatologic disease overlap in prevalence and cardiovascular morbidity. In patients with type 1 diabetes, clinical trials have demonstrated that immune modulators used early in the disease can improve pancreatic function, though their efficacy in adults with longstanding autoimmune diabetes is unknown. In patients with type 2 diabetes, hydroxychloroquine is an effective antihyperglycemic and may be preferred for rheumatologic use in patients with difficult glycemic control. In patients without diabetes, hydroxychloroquine and tumor necrosis factor (TNF) inhibitors have been found to decrease diabetes incidence in observational studies. Additionally, dapsone and sulfasalazine alter erythrocyte survival resulting in inaccurate HbA1c values. These multifaceted effects of immune modulators create a need for coordinated care between providers treating patients with diabetes to individualize medication selection and prevent hypoglycemic events. More research is needed to determine the long-term outcomes of immune modulators in patients with diabetes.
Literature
1.
go back to reference Imboden JB, Hellmann DB, Stone JH. Current diagnosis and treatment rheumatology. 3rd ed. New York: McGraw-Hill Medical; 2012. Imboden JB, Hellmann DB, Stone JH. Current diagnosis and treatment rheumatology. 3rd ed. New York: McGraw-Hill Medical; 2012.
3.
4.
go back to reference Han C, Robinson Jr DW, Hackett MV, Paramore LC, Fraeman KH, Bala MV. Cardiovascular disease and risk factors in patients with rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis. J Rheumatol. 2006;33(11):2167–72.PubMed Han C, Robinson Jr DW, Hackett MV, Paramore LC, Fraeman KH, Bala MV. Cardiovascular disease and risk factors in patients with rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis. J Rheumatol. 2006;33(11):2167–72.PubMed
9.
go back to reference Agner T, Damm P, Binder C. Remission in IDDM: prospective study of basal C-peptide and insulin dose in 268 consecutive patients. Diabetes Care. 1987;10(2):164–9.PubMedCrossRef Agner T, Damm P, Binder C. Remission in IDDM: prospective study of basal C-peptide and insulin dose in 268 consecutive patients. Diabetes Care. 1987;10(2):164–9.PubMedCrossRef
10.
12.
go back to reference Palmer JP, Fleming GA, Greenbaum CJ, Herold KC, Jansa LD, Kolb H, et al. C-peptide is the appropriate outcome measure for type 1 diabetes clinical trials to preserve beta-cell function: report of an ADA workshop, 21–22 October 2001. Diabetes. 2004;53(1):250–64.PubMedCrossRef Palmer JP, Fleming GA, Greenbaum CJ, Herold KC, Jansa LD, Kolb H, et al. C-peptide is the appropriate outcome measure for type 1 diabetes clinical trials to preserve beta-cell function: report of an ADA workshop, 21–22 October 2001. Diabetes. 2004;53(1):250–64.PubMedCrossRef
13.••
go back to reference Rigby MR, Harris KM, Pinckney A, DiMeglio LA, Rendell MS, Felner EI, et al. Alefacept provides sustained clinical and immunological effects in new-onset type 1 diabetes patients. J Clin Invest. 2015;125(8):3285–96. doi:10.1172/JCI81722. This trial demonstrates that alafecept has beneficial effects on recent onset type 1 diabetes with no increase in adverse events.PubMedPubMedCentralCrossRef Rigby MR, Harris KM, Pinckney A, DiMeglio LA, Rendell MS, Felner EI, et al. Alefacept provides sustained clinical and immunological effects in new-onset type 1 diabetes patients. J Clin Invest. 2015;125(8):3285–96. doi:10.​1172/​JCI81722. This trial demonstrates that alafecept has beneficial effects on recent onset type 1 diabetes with no increase in adverse events.PubMedPubMedCentralCrossRef
15.
16.
go back to reference Cook JJ, Hudson I, Harrison LC, Dean B, Colman PG, Werther GA, et al. Double-blind controlled trial of azathioprine in children with newly diagnosed type I diabetes. Diabetes. 1989;38(6):779–83.PubMedCrossRef Cook JJ, Hudson I, Harrison LC, Dean B, Colman PG, Werther GA, et al. Double-blind controlled trial of azathioprine in children with newly diagnosed type I diabetes. Diabetes. 1989;38(6):779–83.PubMedCrossRef
17.
go back to reference Harrison LC, Colman PG, Dean B, Baxter R, Martin FI. Increase in remission rate in newly diagnosed type I diabetic subjects treated with azathioprine. Diabetes. 1985;34(12):1306–8.PubMedCrossRef Harrison LC, Colman PG, Dean B, Baxter R, Martin FI. Increase in remission rate in newly diagnosed type I diabetic subjects treated with azathioprine. Diabetes. 1985;34(12):1306–8.PubMedCrossRef
18.
go back to reference Moncada E, Subira ML, Oleaga A, Goni F, Sanchez-Ibarrola A, Monreal M, et al. Insulin requirements and residual beta-cell function 12 months after concluding immunotherapy in type I diabetic patients treated with combined azathioprine and thymostimulin administration for one year. J Autoimmun. 1990;3(5):625–38.PubMedCrossRef Moncada E, Subira ML, Oleaga A, Goni F, Sanchez-Ibarrola A, Monreal M, et al. Insulin requirements and residual beta-cell function 12 months after concluding immunotherapy in type I diabetic patients treated with combined azathioprine and thymostimulin administration for one year. J Autoimmun. 1990;3(5):625–38.PubMedCrossRef
20.
go back to reference Das UN. Colchicine in diabetes mellitus. J Assoc Physicians India. 1993;41(4):213.PubMed Das UN. Colchicine in diabetes mellitus. J Assoc Physicians India. 1993;41(4):213.PubMed
22.
go back to reference Magnasco A, Rossi A, Catarsi P, Gusmano R, Ginevri F, Perfumo F, et al. Cyclosporin and organ specific toxicity: clinical aspects, pharmacogenetics and perspectives. Curr Clin Pharmacol. 2008;3(3):166–73.PubMedCrossRef Magnasco A, Rossi A, Catarsi P, Gusmano R, Ginevri F, Perfumo F, et al. Cyclosporin and organ specific toxicity: clinical aspects, pharmacogenetics and perspectives. Curr Clin Pharmacol. 2008;3(3):166–73.PubMedCrossRef
23.
go back to reference The Canadian-European Randomized Trial Group. Cyclosporin-induced remission of IDDM after early intervention. Association of 1 yr of cyclosporin treatment with enhanced insulin secretion. Diabetes. 1988;37(11):1574–82.CrossRef The Canadian-European Randomized Trial Group. Cyclosporin-induced remission of IDDM after early intervention. Association of 1 yr of cyclosporin treatment with enhanced insulin secretion. Diabetes. 1988;37(11):1574–82.CrossRef
24.
go back to reference Skyler JS, Rabinovitch A, Group MCDS. Cyclosporine in recent onset type I diabetes mellitus. Effects on islet beta cell function. J Diabetes Complications. 1992;6(2):77–88.PubMedCrossRef Skyler JS, Rabinovitch A, Group MCDS. Cyclosporine in recent onset type I diabetes mellitus. Effects on islet beta cell function. J Diabetes Complications. 1992;6(2):77–88.PubMedCrossRef
25.
go back to reference Chase HP, Butler-Simon N, Garg SK, Hayward A, Klingensmith GJ, Hamman RF, et al. Cyclosporine A for the treatment of new-onset insulin-dependent diabetes mellitus. Pediatrics. 1990;85(3):241–5.PubMed Chase HP, Butler-Simon N, Garg SK, Hayward A, Klingensmith GJ, Hamman RF, et al. Cyclosporine A for the treatment of new-onset insulin-dependent diabetes mellitus. Pediatrics. 1990;85(3):241–5.PubMed
26.
go back to reference Feutren G, Papoz L, Assan R, Vialettes B, Karsenty G, Vexiau P, et al. Cyclosporin increases the rate and length of remissions in insulin-dependent diabetes of recent onset. Results of a multicentre double-blind trial. Lancet. 1986;2(8499):119–24.PubMedCrossRef Feutren G, Papoz L, Assan R, Vialettes B, Karsenty G, Vexiau P, et al. Cyclosporin increases the rate and length of remissions in insulin-dependent diabetes of recent onset. Results of a multicentre double-blind trial. Lancet. 1986;2(8499):119–24.PubMedCrossRef
27.
go back to reference O’Brien D, Butler N, Chase HP, Hammon R, Hayward A, Klingensmith G, et al. Cyclosporin A in treatment of new-onset type I diabetes mellitus. Diabetes Care. 1988;11(3):297.PubMedCrossRef O’Brien D, Butler N, Chase HP, Hammon R, Hayward A, Klingensmith G, et al. Cyclosporin A in treatment of new-onset type I diabetes mellitus. Diabetes Care. 1988;11(3):297.PubMedCrossRef
28.
go back to reference Dupre J, Stiller CR, Gent M, Donner A, von Graffenreid B, Murphy G, et al. Effects of immunosuppression with cyclosporine in insulin-dependent diabetes mellitus of recent onset: the Canadian open study at 44 months. Transplant Proc. 1988;20(3 Suppl 4):184–92.PubMed Dupre J, Stiller CR, Gent M, Donner A, von Graffenreid B, Murphy G, et al. Effects of immunosuppression with cyclosporine in insulin-dependent diabetes mellitus of recent onset: the Canadian open study at 44 months. Transplant Proc. 1988;20(3 Suppl 4):184–92.PubMed
29.
go back to reference Stiller CR, Dupre J, Gent M, Jenner MR, Keown PA, Laupacis A, et al. Effects of cyclosporine immunosuppression in insulin-dependent diabetes mellitus of recent onset. Science. 1984;223(4643):1362–7.PubMedCrossRef Stiller CR, Dupre J, Gent M, Jenner MR, Keown PA, Laupacis A, et al. Effects of cyclosporine immunosuppression in insulin-dependent diabetes mellitus of recent onset. Science. 1984;223(4643):1362–7.PubMedCrossRef
30.
32.
go back to reference Fleming RA. An overview of cyclophosphamide and ifosfamide pharmacology. Pharmacotherapy. 1997;17(5 Pt 2):146S–54S.PubMed Fleming RA. An overview of cyclophosphamide and ifosfamide pharmacology. Pharmacotherapy. 1997;17(5 Pt 2):146S–54S.PubMed
33.
34.
go back to reference Chang DJ, Lamothe M, Stevens RM, Sigal LH. Dapsone in rheumatoid arthritis. Semin Arthritis Rheum. 1996;25(6):390–403.PubMedCrossRef Chang DJ, Lamothe M, Stevens RM, Sigal LH. Dapsone in rheumatoid arthritis. Semin Arthritis Rheum. 1996;25(6):390–403.PubMedCrossRef
35.
go back to reference Degowin RL, Eppes RB, Powell RD, Carson PE. The haemolytic effects of diaphenylsulfone (DDS) in normal subjects and in those with glucose-6-phosphate-dehydrogenase deficiency. Bull World Health Organ. 1966;35(2):165–79.PubMedPubMedCentral Degowin RL, Eppes RB, Powell RD, Carson PE. The haemolytic effects of diaphenylsulfone (DDS) in normal subjects and in those with glucose-6-phosphate-dehydrogenase deficiency. Bull World Health Organ. 1966;35(2):165–79.PubMedPubMedCentral
36.
go back to reference Halim NK, Ogbeide E. Haematological alterations in leprosy patients treated with dapsone. East Afr Med J. 2002;79(2):100–2.PubMedCrossRef Halim NK, Ogbeide E. Haematological alterations in leprosy patients treated with dapsone. East Afr Med J. 2002;79(2):100–2.PubMedCrossRef
45.
go back to reference van Vollenhoven RF. Corticosteroids in rheumatic disease. Understanding their effects is key to their use. Postgrad Med. 1998;103(2):137–42.PubMedCrossRef van Vollenhoven RF. Corticosteroids in rheumatic disease. Understanding their effects is key to their use. Postgrad Med. 1998;103(2):137–42.PubMedCrossRef
47.•
go back to reference Liu XX, Zhu XM, Miao Q, Ye HY, Zhang ZY, Li YM. Hyperglycemia induced by glucocorticoids in nondiabetic patients: a meta-analysis. Ann Nutr Metab. 2014;65(4):324–32. doi:10.1159/000365892. This is a meta-analysis of the incidence of hyperglycemia and new-onset diabetes due to glucocorticoids in non-diabetic patients.PubMedCrossRef Liu XX, Zhu XM, Miao Q, Ye HY, Zhang ZY, Li YM. Hyperglycemia induced by glucocorticoids in nondiabetic patients: a meta-analysis. Ann Nutr Metab. 2014;65(4):324–32. doi:10.​1159/​000365892. This is a meta-analysis of the incidence of hyperglycemia and new-onset diabetes due to glucocorticoids in non-diabetic patients.PubMedCrossRef
48.
go back to reference Mistura L, Beccaria L, Meschi F, Flores D’Arcais A, Pellini C, Puzzovio M, et al. Prednisone treatment in newly diagnosed type I diabetic children: 1-yr follow-up. Diabetes Care. 1987;10(1):39–43.PubMedCrossRef Mistura L, Beccaria L, Meschi F, Flores D’Arcais A, Pellini C, Puzzovio M, et al. Prednisone treatment in newly diagnosed type I diabetic children: 1-yr follow-up. Diabetes Care. 1987;10(1):39–43.PubMedCrossRef
49.
go back to reference Fox RI. Mechanism of action of hydroxychloroquine as an antirheumatic drug. Semin Arthritis Rheum. 1993;23(2 Suppl 1):82–91.PubMedCrossRef Fox RI. Mechanism of action of hydroxychloroquine as an antirheumatic drug. Semin Arthritis Rheum. 1993;23(2 Suppl 1):82–91.PubMedCrossRef
52.
go back to reference Winter EM, Schrander-van der Meer A, Eustatia-Rutten C, Janssen M (2011) Hydroxychloroquine as a glucose lowering drug. BMJ Case Rep 2011. doi:10.1136/bcr.06.2011.4393 Winter EM, Schrander-van der Meer A, Eustatia-Rutten C, Janssen M (2011) Hydroxychloroquine as a glucose lowering drug. BMJ Case Rep 2011. doi:10.1136/bcr.06.2011.4393
53.
go back to reference Kang L, Mikuls TR, O’Dell JR (2009) Hydroxychloroquine: a diabetic drug in disguise? BMJ Case Rep 2009. doi:10.1136/bcr.08.2008.0654 Kang L, Mikuls TR, O’Dell JR (2009) Hydroxychloroquine: a diabetic drug in disguise? BMJ Case Rep 2009. doi:10.1136/bcr.08.2008.0654
54.
go back to reference Shojania K, Koehler BE, Elliott T. Hypoglycemia induced by hydroxychloroquine in a type II diabetic treated for polyarthritis. J Rheumatol. 1999;26(1):195–6.PubMed Shojania K, Koehler BE, Elliott T. Hypoglycemia induced by hydroxychloroquine in a type II diabetic treated for polyarthritis. J Rheumatol. 1999;26(1):195–6.PubMed
56.
go back to reference Gerstein HC, Thorpe KE, Taylor DW, Haynes RB. 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):209–19.PubMedCrossRef Gerstein HC, Thorpe KE, Taylor DW, Haynes RB. 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):209–19.PubMedCrossRef
57.
go back to reference Quatraro A, Consoli G, Magno M, Caretta F, Nardozza A, Ceriello A, et al. Hydroxychloroquine in decompensated, treatment-refractory noninsulin-dependent diabetes mellitus. A new job for an old drug? Ann Intern Med. 1990;112(9):678–81.PubMedCrossRef Quatraro A, Consoli G, Magno M, Caretta F, Nardozza A, Ceriello A, et al. Hydroxychloroquine in decompensated, treatment-refractory noninsulin-dependent diabetes mellitus. A new job for an old drug? Ann Intern Med. 1990;112(9):678–81.PubMedCrossRef
58.•
go back to reference Pareek A, Chandurkar N, Thomas N, Viswanathan V, Deshpande A, Gupta OP, et al. Efficacy and safety of hydroxychloroquine in the treatment of type 2 diabetes mellitus: a double blind, randomized comparison with pioglitazone. Curr Med Res Opin. 2014;30(7):1257–66. doi:10.1185/03007995.2014.909393. This trial compares hydroxychloroquine to pioglitazone in patients with type 2 diabetes demonstrating non-inferiority of hydroxychloroquine in reducing HbA1c, and improved lipid profiles in the hydroxychloroquine arm.PubMedCrossRef Pareek A, Chandurkar N, Thomas N, Viswanathan V, Deshpande A, Gupta OP, et al. Efficacy and safety of hydroxychloroquine in the treatment of type 2 diabetes mellitus: a double blind, randomized comparison with pioglitazone. Curr Med Res Opin. 2014;30(7):1257–66. doi:10.​1185/​03007995.​2014.​909393. This trial compares hydroxychloroquine to pioglitazone in patients with type 2 diabetes demonstrating non-inferiority of hydroxychloroquine in reducing HbA1c, and improved lipid profiles in the hydroxychloroquine arm.PubMedCrossRef
59.
go back to reference Rekedal LR, Massarotti E, Garg R, Bhatia R, Gleeson T, Lu B, et al. Changes in glycosylated hemoglobin after initiation of hydroxychloroquine or methotrexate treatment in diabetes patients with rheumatic diseases. Arthritis Rheum. 2010;62(12):3569–73. doi:10.1002/art.27703.PubMedPubMedCentralCrossRef Rekedal LR, Massarotti E, Garg R, Bhatia R, Gleeson T, Lu B, et al. Changes in glycosylated hemoglobin after initiation of hydroxychloroquine or methotrexate treatment in diabetes patients with rheumatic diseases. Arthritis Rheum. 2010;62(12):3569–73. doi:10.​1002/​art.​27703.PubMedPubMedCentralCrossRef
62.
go back to reference Solomon DH, Massarotti E, Garg R, Liu J, Canning C, Schneeweiss S. Association between disease-modifying antirheumatic drugs and diabetes risk in patients with rheumatoid arthritis and psoriasis. JAMA. 2011;305(24):2525–31. doi:10.1001/jama.2011.878.PubMedCrossRef Solomon DH, Massarotti E, Garg R, Liu J, Canning C, Schneeweiss S. Association between disease-modifying antirheumatic drugs and diabetes risk in patients with rheumatoid arthritis and psoriasis. JAMA. 2011;305(24):2525–31. doi:10.​1001/​jama.​2011.​878.PubMedCrossRef
63.•
go back to reference Chen YM, Lin CH, Lan TH, Chen HH, Chang SN, Chen YH, et al. 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):1244–9. doi:10.1093/rheumatology/keu451. This retrospective cohort study found lower diabetes incidence associated with higher exposure to hydroxychloroquine in patients with systemic lupus erythematosus using a nation-wide registry in Taiwan.CrossRef Chen YM, Lin CH, Lan TH, Chen HH, Chang SN, Chen YH, et al. 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):1244–9. doi:10.​1093/​rheumatology/​keu451. This retrospective cohort study found lower diabetes incidence associated with higher exposure to hydroxychloroquine in patients with systemic lupus erythematosus using a nation-wide registry in Taiwan.CrossRef
65.•
go back to reference Abdel-Hamid AA, El-Firgany Ael D. Hydroxychloroquine hindering of diabetic isletopathy carries its signature on the inflammatory cytokines. J Mol Histol. 2016;47(2):183–93. doi:10.1007/s10735-016-9664-5. This study examines the histologic and immunologic effects of hydroxychloroquine in a rat models of pancreatic endocrine failure.PubMedCrossRef Abdel-Hamid AA, El-Firgany Ael D. Hydroxychloroquine hindering of diabetic isletopathy carries its signature on the inflammatory cytokines. J Mol Histol. 2016;47(2):183–93. doi:10.​1007/​s10735-016-9664-5. This study examines the histologic and immunologic effects of hydroxychloroquine in a rat models of pancreatic endocrine failure.PubMedCrossRef
70.
72.
go back to reference Gottlieb PA, Quinlan S, Krause Steinrauf H, Greenbaum CJ, Wilson DM, Rodriguez H, et al. Failure to preserve beta-cell function with mycophenolate mofetil and daclizumab combined therapy in patients with new-onset type 1 diabetes. Diabetes Care. 2010;33(4):826–32. doi:10.2337/dc09-1349.PubMedPubMedCentralCrossRef Gottlieb PA, Quinlan S, Krause Steinrauf H, Greenbaum CJ, Wilson DM, Rodriguez H, et al. Failure to preserve beta-cell function with mycophenolate mofetil and daclizumab combined therapy in patients with new-onset type 1 diabetes. Diabetes Care. 2010;33(4):826–32. doi:10.​2337/​dc09-1349.PubMedPubMedCentralCrossRef
74.
go back to reference Smedegard G, Bjork J. Sulphasalazine: mechanism of action in rheumatoid arthritis. Br J Rheumatol. 1995;34 Suppl 2:7–15.PubMedCrossRef Smedegard G, Bjork J. Sulphasalazine: mechanism of action in rheumatoid arthritis. Br J Rheumatol. 1995;34 Suppl 2:7–15.PubMedCrossRef
75.
go back to reference Taffet SL, Das KM. Sulfasalazine. Adverse effects and desensitization. Dig Dis Sci. 1983;28(9):833–42.PubMedCrossRef Taffet SL, Das KM. Sulfasalazine. Adverse effects and desensitization. Dig Dis Sci. 1983;28(9):833–42.PubMedCrossRef
76.
go back to reference Tack CJ, Wetzels JF. Decreased HbA1c levels due to sulfonamide-induced hemolysis in two IDDM patients. Diabetes Care. 1996;19(7):775–6.PubMedCrossRef Tack CJ, Wetzels JF. Decreased HbA1c levels due to sulfonamide-induced hemolysis in two IDDM patients. Diabetes Care. 1996;19(7):775–6.PubMedCrossRef
77.
go back to reference Haas RM, Li P, Chu JW. Glucose-lowering effects of sulfasalazine in type 2 diabetes. Diabetes Care. 2005;28(9):2238–9.PubMedCrossRef Haas RM, Li P, Chu JW. Glucose-lowering effects of sulfasalazine in type 2 diabetes. Diabetes Care. 2005;28(9):2238–9.PubMedCrossRef
79.
go back to reference Mastrandrea L, Yu J, Behrens T, Buchlis J, Albini C, Fourtner S, et al. Etanercept treatment in children with new-onset type 1 diabetes: pilot randomized, placebo-controlled, double-blind study. Diabetes Care. 2009;32(7):1244–9. doi:10.2337/dc09-0054.PubMedPubMedCentralCrossRef Mastrandrea L, Yu J, Behrens T, Buchlis J, Albini C, Fourtner S, et al. Etanercept treatment in children with new-onset type 1 diabetes: pilot randomized, placebo-controlled, double-blind study. Diabetes Care. 2009;32(7):1244–9. doi:10.​2337/​dc09-0054.PubMedPubMedCentralCrossRef
81.
go back to reference Olivieri AN, Iafusco D, Mellos A, Zanfardino A, Mauro A, Granato C, et al. Refractory rheumatoid factor positive polyarthritis in a female adolescent already suffering from type 1 diabetes mellitus and Hashimoto’s thyroiditis successfully treated with etanercept. Ital J Pediatr. 2013;39:64. doi:10.1186/1824-7288-39-64.PubMedPubMedCentralCrossRef Olivieri AN, Iafusco D, Mellos A, Zanfardino A, Mauro A, Granato C, et al. Refractory rheumatoid factor positive polyarthritis in a female adolescent already suffering from type 1 diabetes mellitus and Hashimoto’s thyroiditis successfully treated with etanercept. Ital J Pediatr. 2013;39:64. doi:10.​1186/​1824-7288-39-64.PubMedPubMedCentralCrossRef
83.
go back to reference van Eijk IC, Peters MJ, Nurmohamed MT, van Deutekom AW, Dijkmans BA, Simsek S. Decrease of fructosamine levels during treatment with adalimumab in patients with both diabetes and rheumatoid arthritis. Eur J Endocrinol. 2007;156(3):291–3. doi:10.1530/EJE-06-0693.PubMedCrossRef van Eijk IC, Peters MJ, Nurmohamed MT, van Deutekom AW, Dijkmans BA, Simsek S. Decrease of fructosamine levels during treatment with adalimumab in patients with both diabetes and rheumatoid arthritis. Eur J Endocrinol. 2007;156(3):291–3. doi:10.​1530/​EJE-06-0693.PubMedCrossRef
88.
go back to reference Singh JA, Wells GA, Christensen R, Tanjong Ghogomu E, Maxwell L, Macdonald JK, et al. Adverse effects of biologics: a network meta-analysis and Cochrane overview. Cochrane Database Syst Rev. 2011;2:CD008794. doi:10.1002/14651858.CD008794.pub2.PubMed Singh JA, Wells GA, Christensen R, Tanjong Ghogomu E, Maxwell L, Macdonald JK, et al. Adverse effects of biologics: a network meta-analysis and Cochrane overview. Cochrane Database Syst Rev. 2011;2:CD008794. doi:10.​1002/​14651858.​CD008794.​pub2.PubMed
90.
go back to reference Farrokhi F, Taylor HC, McBride NM. Etanercept-induced hypoglycemia and improved glycemic control in a patient with type 2 diabetes. Endocr Pract. 2011;17(2):306–7.PubMedCrossRef Farrokhi F, Taylor HC, McBride NM. Etanercept-induced hypoglycemia and improved glycemic control in a patient with type 2 diabetes. Endocr Pract. 2011;17(2):306–7.PubMedCrossRef
92.
go back to reference Wambier CG, Foss-Freitas MC, Paschoal RS, Tomazini MV, Simao JC, Foss MC, et al. Severe hypoglycemia after initiation of anti-tumor necrosis factor therapy with etanercept in a patient with generalized pustular psoriasis and type 2 diabetes mellitus. J Am Acad Dermatol. 2009;60(5):883–5. doi:10.1016/j.jaad.2008.10.009.PubMedCrossRef Wambier CG, Foss-Freitas MC, Paschoal RS, Tomazini MV, Simao JC, Foss MC, et al. Severe hypoglycemia after initiation of anti-tumor necrosis factor therapy with etanercept in a patient with generalized pustular psoriasis and type 2 diabetes mellitus. J Am Acad Dermatol. 2009;60(5):883–5. doi:10.​1016/​j.​jaad.​2008.​10.​009.PubMedCrossRef
94.
go back to reference Yazdani-Biuki B, Stelzl H, Brezinschek HP, Hermann J, Mueller T, Krippl P, et al. Improvement of insulin sensitivity in insulin resistant subjects during prolonged treatment with the anti-TNF-alpha antibody infliximab. Eur J Clin Invest. 2004;34(9):641–2. doi:10.1111/j.1365-2362.2004.01390.x.PubMedCrossRef Yazdani-Biuki B, Stelzl H, Brezinschek HP, Hermann J, Mueller T, Krippl P, et al. Improvement of insulin sensitivity in insulin resistant subjects during prolonged treatment with the anti-TNF-alpha antibody infliximab. Eur J Clin Invest. 2004;34(9):641–2. doi:10.​1111/​j.​1365-2362.​2004.​01390.​x.PubMedCrossRef
95.
go back to reference Yazdani-Biuki B, Mueller T, Brezinschek HP, Hermann J, Graninger W, Wascher TC. Relapse of diabetes after interruption of chronic administration of anti-tumor necrosis factor-alpha antibody infliximab: a case observation. Diabetes Care. 2006;29(7):1712–3. doi:10.2337/dc06-0636.PubMedCrossRef Yazdani-Biuki B, Mueller T, Brezinschek HP, Hermann J, Graninger W, Wascher TC. Relapse of diabetes after interruption of chronic administration of anti-tumor necrosis factor-alpha antibody infliximab: a case observation. Diabetes Care. 2006;29(7):1712–3. doi:10.​2337/​dc06-0636.PubMedCrossRef
98.•
go back to reference Orban T, Bundy B, Becker DJ, Dimeglio LA, Gitelman SE, Goland R, 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. This follow-up study to an RCT of abatacept in recent onset type 1 diabetes [97] demonstrates persistent improvements in pancreatic function one year after abatacept was stopped.PubMedPubMedCentralCrossRef Orban T, Bundy B, Becker DJ, Dimeglio LA, Gitelman SE, Goland R, 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. This follow-up study to an RCT of abatacept in recent onset type 1 diabetes [97] demonstrates persistent improvements in pancreatic function one year after abatacept was stopped.PubMedPubMedCentralCrossRef
99.
go back to reference Chamian F, Lin SL, Lee E, Kikuchi T, Gilleaudeau P, Sullivan-Whalen M, et al. Alefacept (anti-CD2) causes a selective reduction in circulating effector memory T cells (Tem) and relative preservation of central memory T cells (Tcm) in psoriasis. J Transl Med. 2007;5:27. doi:10.1186/1479-5876-5-27.PubMedPubMedCentralCrossRef Chamian F, Lin SL, Lee E, Kikuchi T, Gilleaudeau P, Sullivan-Whalen M, et al. Alefacept (anti-CD2) causes a selective reduction in circulating effector memory T cells (Tem) and relative preservation of central memory T cells (Tcm) in psoriasis. J Transl Med. 2007;5:27. doi:10.​1186/​1479-5876-5-27.PubMedPubMedCentralCrossRef
101.
102.•
go back to reference Moran A, Bundy B, Becker DJ, DiMeglio LA, Gitelman SE, Goland R, 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. This trial of anakinra or canakinumab versus placebo finds no effects on pancreatic function of either drug in patients with recent onset type 1 diabetes.PubMedCrossRef Moran A, Bundy B, Becker DJ, DiMeglio LA, Gitelman SE, Goland R, 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. This trial of anakinra or canakinumab versus placebo finds no effects on pancreatic function of either drug in patients with recent onset type 1 diabetes.PubMedCrossRef
103.
go back to reference van Asseldonk EJ, van Poppel PC, Ballak DB, Stienstra R, Netea MG, Tack CJ. 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.PubMedCrossRef van Asseldonk EJ, van Poppel PC, Ballak DB, Stienstra R, Netea MG, Tack CJ. 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.PubMedCrossRef
104.
106.
107.
go back to reference Hensen J, Howard CP, Walter V, Thuren T. Impact of interleukin-1beta antibody (canakinumab) on glycaemic indicators in patients with type 2 diabetes mellitus: results of secondary endpoints from a randomized, placebo-controlled trial. Diabetes Metab. 2013;39(6):524–31. doi:10.1016/j.diabet.2013.07.003.PubMedCrossRef Hensen J, Howard CP, Walter V, Thuren T. Impact of interleukin-1beta antibody (canakinumab) on glycaemic indicators in patients with type 2 diabetes mellitus: results of secondary endpoints from a randomized, placebo-controlled trial. Diabetes Metab. 2013;39(6):524–31. doi:10.​1016/​j.​diabet.​2013.​07.​003.PubMedCrossRef
109.
go back to reference Pescovitz MD, Greenbaum CJ, Krause-Steinrauf H, Becker DJ, Gitelman SE, Goland R, et al. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N Engl J Med. 2009;361(22):2143–52. doi:10.1056/NEJMoa0904452.PubMedCrossRef Pescovitz MD, Greenbaum CJ, Krause-Steinrauf H, Becker DJ, Gitelman SE, Goland R, et al. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N Engl J Med. 2009;361(22):2143–52. doi:10.​1056/​NEJMoa0904452.PubMedCrossRef
111.
go back to reference Quintana L, Paniagua JA, Gil-Contreras D, Jimenez-Yuste V, Torres A, Velasco F. Improving type 1 diabetes after treatment of immune thrombocytopenia with rituximab: killing two birds with one stone. Diabetes Care. 2010;33(9):e122. doi:10.2337/dc10-0959.PubMedCrossRef Quintana L, Paniagua JA, Gil-Contreras D, Jimenez-Yuste V, Torres A, Velasco F. Improving type 1 diabetes after treatment of immune thrombocytopenia with rituximab: killing two birds with one stone. Diabetes Care. 2010;33(9):e122. doi:10.​2337/​dc10-0959.PubMedCrossRef
113.
go back to reference Ogata A, Morishima A, Hirano T, Hishitani Y, Hagihara K, Shima Y, 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.PubMedCrossRef Ogata A, Morishima A, Hirano T, Hishitani Y, Hagihara K, Shima Y, 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.PubMedCrossRef
114.
go back to reference Steffes MW, Sibley S, Jackson M, Thomas W. Beta-cell function and the development of diabetes-related complications in the diabetes control and complications trial. Diabetes Care. 2003;26(3):832–6.PubMedCrossRef Steffes MW, Sibley S, Jackson M, Thomas W. Beta-cell function and the development of diabetes-related complications in the diabetes control and complications trial. Diabetes Care. 2003;26(3):832–6.PubMedCrossRef
115.
go back to reference Panero F, Novelli G, Zucco C, Fornengo P, Perotto M, Segre O, et al. Fasting plasma C-peptide and micro- and macrovascular complications in a large clinic-based cohort of type 1 diabetic patients. Diabetes Care. 2009;32(2):301–5. doi:10.2337/dc08-1241.PubMedPubMedCentralCrossRef Panero F, Novelli G, Zucco C, Fornengo P, Perotto M, Segre O, et al. Fasting plasma C-peptide and micro- and macrovascular complications in a large clinic-based cohort of type 1 diabetic patients. Diabetes Care. 2009;32(2):301–5. doi:10.​2337/​dc08-1241.PubMedPubMedCentralCrossRef
116.
117.
go back to reference Kobayashi T, Tamemoto K, Nakanishi K, Kato N, Okubo M, Kajio H, et al. Immunogenetic and clinical characterization of slowly progressive IDDM. Diabetes Care. 1993;16(5):780–8.PubMedCrossRef Kobayashi T, Tamemoto K, Nakanishi K, Kato N, Okubo M, Kajio H, et al. Immunogenetic and clinical characterization of slowly progressive IDDM. Diabetes Care. 1993;16(5):780–8.PubMedCrossRef
118.
go back to reference Morris SJ, Wasko MC, Antohe JL, Sartorius JA, Kirchner HL, Dancea S, et al. Hydroxychloroquine use associated with improvement in lipid profiles in rheumatoid arthritis patients. Arthritis Care Res (Hoboken). 2011;63(4):530–4. doi:10.1002/acr.20393.CrossRef Morris SJ, Wasko MC, Antohe JL, Sartorius JA, Kirchner HL, Dancea S, et al. Hydroxychloroquine use associated with improvement in lipid profiles in rheumatoid arthritis patients. Arthritis Care Res (Hoboken). 2011;63(4):530–4. doi:10.​1002/​acr.​20393.CrossRef
119.
go back to reference Solomon DH, Garg R, Lu B, Todd DJ, Mercer E, Norton T, et al. Effect of hydroxychloroquine on insulin sensitivity and lipid parameters in rheumatoid arthritis patients without diabetes mellitus: a randomized, blinded crossover trial. Arthritis Care Res (Hoboken). 2014;66(8):1246–51. doi:10.1002/acr.22285.CrossRef Solomon DH, Garg R, Lu B, Todd DJ, Mercer E, Norton T, et al. Effect of hydroxychloroquine on insulin sensitivity and lipid parameters in rheumatoid arthritis patients without diabetes mellitus: a randomized, blinded crossover trial. Arthritis Care Res (Hoboken). 2014;66(8):1246–51. doi:10.​1002/​acr.​22285.CrossRef
120.
go back to reference Jacobsson LT, Turesson C, Gulfe A, Kapetanovic MC, Petersson IF, Saxne T, et al. Treatment with tumor necrosis factor blockers is associated with a lower incidence of first cardiovascular events in patients with rheumatoid arthritis. J Rheumatol. 2005;32(7):1213–8.PubMed Jacobsson LT, Turesson C, Gulfe A, Kapetanovic MC, Petersson IF, Saxne T, et al. Treatment with tumor necrosis factor blockers is associated with a lower incidence of first cardiovascular events in patients with rheumatoid arthritis. J Rheumatol. 2005;32(7):1213–8.PubMed
Metadata
Title
Immune-Modulating Therapy for Rheumatologic Disease: Implications for Patients with Diabetes
Authors
Scott J. Pilla
Amy Q. Quan
Emily L. Germain-Lee
David B. Hellmann
Nestoras N. Mathioudakis
Publication date
01-10-2016
Publisher
Springer US
Published in
Current Diabetes Reports / Issue 10/2016
Print ISSN: 1534-4827
Electronic ISSN: 1539-0829
DOI
https://doi.org/10.1007/s11892-016-0792-9

Other articles of this Issue 10/2016

Current Diabetes Reports 10/2016 Go to the issue

Pathogenesis of Type 1 Diabetes (A Pugliese, Section Editor)

Biomarkers of β-Cell Stress and Death in Type 1 Diabetes

Lifestyle Management to Reduce Diabetes/Cardiovascular Risk (C Shay and B Conway, Section Editors)

Viral Hepatitis and Diabetes: Clinical Implications of Diabetes Prevention Through Hepatitis Vaccination

Microvascular Complications—Retinopathy (JK Sun and PS Silva, Section Editors)

Fenofibrate and Diabetic Retinopathy

Pharmacologic Treatment of Type 2 Diabetes (HE Lebovitz and G Bahtiyar, Section Editors)

SGLT2 Inhibitors: Benefit/Risk Balance

Obesity (J McCaffery, Section Editor)

Salivary Amylase: Digestion and Metabolic Syndrome

Health Care Delivery Systems and Implementation in Diabetes (EB Morton-Eggleston and ME McDonnell, Section Editors)

Academic Detailing in Diabetes: Using Outreach Education to Improve the Quality of Care

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine