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Research ArticleArticle
Open Access

Higher Prevalence and Degree of Insulin Resistance in Patients with Rheumatoid Arthritis Than in Patients With Systemic Lupus Erythematosus

Juan C. Quevedo-Abeledo, Hiurma Sánchez-Pérez, Beatriz Tejera-Segura, Laura de Armas-Rillo, Soledad Ojeda, Celia Erausquin, Miguel Á. González-Gay and Iván Ferraz-Amaro
The Journal of Rheumatology June 2020, jrheum.200435; DOI: https://doi.org/10.3899/jrheum.200435
Juan C. Quevedo-Abeledo
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Hiurma Sánchez-Pérez
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Beatriz Tejera-Segura
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Laura de Armas-Rillo
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Soledad Ojeda
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Celia Erausquin
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Miguel Á. González-Gay
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Iván Ferraz-Amaro
This work was supported by a grant to Dr. Ferraz-Amaro from the Spanish Ministry of Health, Subdirección General de Evaluación y Fomento de la Investigación, Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016, and by Fondo Europeo de Desarrollo Regional - FEDER - (Fondo de Investigaciones Sanitarias grants PI14/00394, PI17/00083). Prof. González-Gay’s research is supported by the Instituto de Salud Carlos III (ISCIII; Fondo de Investigación Sanitaria grants PI06/0024, PI09/00748, PI12/00060, PI15/00525, PI18/00043) and the ISCIII RETICS programs (RD12/0009 and RD16/0012). J.C. Quevedo-Abeledo, MD, S. Ojeda, PhD, MD, C. Erausquin, PhD, MD, Division of Rheumatology, Hospital Doctor Negrín, Gran Canaria, Spain; H. Sánchez-Pérez, MD, I. Ferraz-Amaro, PhD, MD, Division of Rheumatology, Hospital Universitario de Canarias, Tenerife, Spain; B. Tejera-Segura, PhD, MD, Division of Rheumatology, Hospital Insular de Gran Canaria, Gran Canaria, Spain; L. de Armas-Rillo, PhD, Division of Health Sciences, Universidad Europea de Canarias, Tenerife, Spain; M.Á. González-Gay, PhD, MD, School of Medicine, University of Cantabria, and Division of Rheumatology, Hospital Marqués de Valdecilla, Santander, Spain, and Cardiovascular Pathophysiology and Genomics Research Unit, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. M.Á. González-Gay and I. Ferraz-Amaro share senior authorship of this manuscript. The authors declare that they have no competing interests related to this study. Nevertheless, M.A. Gonzalez-Gay and I. Ferraz-Amaro would like to acknowledge that they received grants/research supports from Abbott, MSD, Jansen, and Roche, as well as consultation fees from company-sponsored speakers bureaus associated with Abbott, Pfizer, Roche, Sanofi, Celgene, and MSD. Address correspondence to Prof. M.Á. González-Gay. Division of Rheumatology, Hospital Universitario Marqués de Valdecilla, IDIVAL, Santander, Spain. Email: miguelaggay@hotmail.com. Or Dr. I. Ferraz-Amaro. Division of Rheumatology, Hospital Universitario de Canarias, 38320 Santa Cruz de Tenerife, Spain. Email: iferrazamaro@hotmail.com. Accepted for publication June 4, 2020.
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Abstract

Objective Since insulin resistance (IR) is highly prevalent in patients with systemic lupus erythematosus (SLE) and rheumatoid arthritis (RA), we aimed to determine whether differences in IR exist between the two conditions.

Methods We conducted a cross-sectional study comprising 413 subjects without diabetes (186 with SLE and 227 with RA). Glucose, insulin, and C-peptide serum levels, as well as IR by the homeostatic model assessment (HOMA2) were studied. A multivariable regression analysis was performed to evaluate the differences in IR indexes between patients with SLE and RA, as well as to determine if IR risk factors or disease-related characteristics are differentially associated with IR in both populations.

Results The insulin:C-peptide molar ratio was upregulated in patients with RA compared to patients with SLE (β 0.009, 95% CI 0.005–0.014, P < 0.001) after multivariable analysis. HOMA2 indexes related to insulin sensitivity (HOMA2-%S) were found to be lower (β –27, 95% CI –46 to –9, P = 0.004) and β cell function (HOMA2-%B) showed higher IR indexes (β 38, 95% CI 23–52, P < 0.001) in RA than in SLE patients after multivariable analysis. Patients with RA more often fulfilled the definition of IR than those with SLE (OR 2.15, 95% CI 1.25–3.69, P = 0.005). The size effect of IR factors on IR indexes was found to be equal in both diseases.

Conclusion IR sensitivity is lower and β cell function is higher in RA than in SLE patients. The fact that traditional IR factors have an equal effect on IR in both SLE and RA supports the contention that these differences are related to the diseases themselves.

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Higher Prevalence and Degree of Insulin Resistance in Patients with Rheumatoid Arthritis Than in Patients With Systemic Lupus Erythematosus
Juan C. Quevedo-Abeledo, Hiurma Sánchez-Pérez, Beatriz Tejera-Segura, Laura de Armas-Rillo, Soledad Ojeda, Celia Erausquin, Miguel Á. González-Gay, Iván Ferraz-Amaro
The Journal of Rheumatology Jun 2020, jrheum.200435; DOI: 10.3899/jrheum.200435

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Higher Prevalence and Degree of Insulin Resistance in Patients with Rheumatoid Arthritis Than in Patients With Systemic Lupus Erythematosus
Juan C. Quevedo-Abeledo, Hiurma Sánchez-Pérez, Beatriz Tejera-Segura, Laura de Armas-Rillo, Soledad Ojeda, Celia Erausquin, Miguel Á. González-Gay, Iván Ferraz-Amaro
The Journal of Rheumatology Jun 2020, jrheum.200435; DOI: 10.3899/jrheum.200435
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