Abstract
The metabolic characteristics of rheumatoid arthritis (RA) or diabetes mellitus (DM) have been studied, but the metabolic abnormalities of RA patients complicated with DM are not completely understood. Therefore, we recruited RA patients with DM to investigate the metabolic abnormalities in these patients. We collected data of RA patients with DM and age- and sex-matched RA and DM patients from Changhai Hospital’s electronic medical record system. Data of demographically matched healthy controls were also collected from the health management system of the Hangzhou Sanatorium of People’s Liberation Army. Blood pressure, uric acid, glucose, and lipid levels were compared. The clinical data of RA with DM (n = 104), DM (n = 100), and RA (n = 100) patients and healthy controls (n = 100) were collected and compared. RA patients with DM had higher blood pressure and lower high-density lipoprotein cholesterol levels than the other three groups, a higher triglycerides (TG) level than healthy controls and RA patients, and a lower TG level than DM patients. RA patients with DM exhibited a relatively high proportion of metabolic abnormalities based on existing standards. Our study examined metabolic abnormalities in RA patients with DM for the first time, and our results suggest that clinicians should pay more attention to the metabolic abnormalities of RA patients with DM.
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Liu XZ, Fan J, Qi K, Liu SP, Xu WD, Gao Y, Gu XD, Li J, Bai CG, Shi YQ, Zhang LL, Zhao DB (2017) Dishevelled2 promotes apoptosis and inhibits inflammatory cytokine secretion in rheumatoid arthritis fibroblast-like synoviocytes through crosstalk with the NF-κB pathway. Oncotarget 8:12649–12663
Aviña-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D (2008) Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Rheum 59:1690–1697
Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE (2005) Cardiovascular death in rheumatoid arthritis: a population-based study. Arthritis Rheum 52:722–732
Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE, Stampfer MJ, Curhan GC (2003) Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 107:1303–1307
Amaya-Amaya J, Sarmiento-Monroy JC, Mantilla RD, Pineda-Tamayo R, Rojas-Villarraga A, Anaya JM (2013) Novel risk factors for cardiovascular disease in rheumatoid arthritis. Immunol Res 56:267–286
Wibetoe G, Ikdahl E, Rollefstad S, Olsen IC, Bergsmark K, Kvien TK, Salberg A, Soldal DM, Bakland G, Lexberg Å, Fevang BT, Gulseth HC, Haugeberg G, Semb AG (2017) Cardiovascular disease risk profiles in inflammatory joint disease entities. Arthritis Res Ther 19:153
Solomon DH, Love TJ, Canning C, Schneeweiss S (2010) Risk of diabetes among patients with rheumatoid arthritis, psoriatic arthritis and psoriasis. Ann Rheum Dis 69:2114–2117
Barber CE, Smith A, Esdaile JM, Barnabe C, Martin LO, Faris P, Hazlewood G, Noormohamed R, Alvarez N, Mancini GB, Lacaille D, Keeling S, Aviña-Zubieta JA, Marshall D (2015) Best practices for cardiovascular disease prevention in rheumatoid arthritis: a systematic review of guideline recommendations and quality indicators. Arthritis Care Res (Hoboken) 67:169–179
Agca R, Heslinga SC, Rollefstad S, Heslinga M, McInnes IB, Peters MJ, Kvien TK, Dougados M, Radner H, Atzeni F, Primdahl J, Södergren A, Wallberg Jonsson S, van Rompay J, Zabalan C, Pedersen TR, Jacobsson L, de Vlam K, Gonzalez-Gay MA, Semb AG, Kitas GD, Smulders YM, Szekanecz Z, Sattar N, Symmons DP, Nurmohamed MT (2017) EULAR recommendations for cardiovascular disease risk management in patients with rheumatoid arthritis and other forms of inflammatory joint disorders: 2015/2016 update. Ann Rheum Dis 76:17–28
Ji L, Hu D, Pan C, Weng J, Huo Y, Ma C, Mu Y, Hao C, Ji Q, Ran X, Su B, Zhuo H, Fox KA, Weber M, Zhang D, CCMR Advisory Board, CCMR-3B STUDY Investigators (2013) Primacy of the 3B approach to control risk factors for cardiovascular disease in type 2 diabetes patients. Am J Med 126:925.e11–925.e22
Bartels CM, Kind AJ, Thorpe CT, Everett CM, Cook RJ, McBride PE, Smith MA (2012) Lipid testing in patients with rheumatoid arthritis and key cardiovascular-related comorbidities: a medicare analysis. Semin Arthritis Rheum 42:9–16
Yang W, Lu J, Weng J, Jia W, Ji L, Xiao J, Shan Z, Liu J, Tian H, Ji Q, Zhu D, Ge J, Lin L, Chen L, Guo X, Zhao Z, Li Q, Zhou Z, Shan G, He J, China National Diabetes and Metabolic Disorders Study Group (2010) Prevalence of diabetes among men and women in China. N Engl J Med 362:1090–1101
van Halm VP, Peters MJ, Voskuyl AE, Boers M, Lems WF, Visser M, Stehouwer CD, Spijkerman AM, Dekker JM, Nijpels G, Heine RJ, Bouter LM, Smulders YM, Dijkmans BA, Nurmohamed MT (2009) Rheumatoid arthritis versus diabetes as a risk factor for cardiovascular disease: a cross-sectional study, the CARRE Investigation. Ann Rheum Dis 68:1395–1400
Peters MJ, van Halm VP, Voskuyl AE, Smulders YM, Boers M, Lems WF, Visser M, Stehouwer CD, Dekker JM, Nijpels G, Heine R, Dijkmans BA (2009) Does rheumatoid arthritis equal diabetes mellitus as an independent risk factor for cardiovascular disease? A prospective study. Arthritis Rheum 61:1571–1579
Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324
Graf J, Scherzer R, Grunfeld C, Imboden J (2009) Levels of C-reactive protein associated with high and very high cardiovascular risk are prevalent in patients with rheumatoid arthritis. PLoS One 4:e6242
McCarey DW, McInnes IB, Madhok R, Hampson R, Scherbakov O, Ford I, Capell HA, Sattar N (2004) Trial of Atorvastatin in Rheumatoid Arthritis (TARA): double-blind, randomised placebo-controlled trial. Lancet 363:2015–2021
Expert Consultation WHO (2004) Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363:157–163
Innala L, Möller B, Ljung L, Magnusson S, Smedby T, Södergren A, Öhman ML, Rantapää-Dahlqvist S, Wållberg-Jonsson S (2011) Cardiovascular events in early RA are a result of inflammatory burden and traditional risk factors: a five year prospective study. Arthritis Res Ther 13:R131
Gabriel SE, Crowson CS (2012) Risk factors for cardiovascular disease in rheumatoid arthritis. Curr Opin Rheumatol 24:171–176
Chinese adult dyslipidemia Prevention Guide Revision Joint Committee (2016) Chinese adult dyslipidemia prevention guide (2016 revised edition). Chinese Circulation Journal 31:937–953 (In Chinese)
Han C, Robinson DW Jr, Hackett MV, Paramore LC, Fraeman KH, Bala MV (2006) Cardiovascular disease and risk factors in patients with rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis. J Rheumatol 33:2167–2172
Solomon DH, Curhan GC, Rimm EB, Cannuscio CC, Karlson EW (2004) Cardiovascular risk factors in women with and without rheumatoid arthritis. Arthritis Rheum 50:3444–3449
Ljung L, Rantapää-Dahlqvist S (2016) Abdominal obesity, gender and the risk of rheumatoid arthritis—a nested case-control study. Arthritis Res Ther 18:277
Tedeschi SK, Cui J, Arkema EV, Robinson WH, Sokolove J, Lingampalli N, Sparks JA, Karlson EW, Costenbader KH (2016) Elevated BMI and antibodies to citrullinated proteins interact to increase rheumatoid arthritis risk and shorten time to diagnosis: a nested case-control study of women in the Nurses’ Health Studies. Semin Arthritis Rheum S0049-0172:30268–30262
Unriza-Puin S, Bautista-Molano W, Lafaurie GI, Valle-Oñate R, Chalem P, Chila-Moreno L, Bello-Gualtero JM, Romero-Sánchez C (2016) Are obesity, ACPAs and periodontitis conditions that influence the risk of developing rheumatoid arthritis in first-degree relatives? Clin Rheumatol [Epub ahead of print]
Albrecht K, Richter A, Callhoff J, Huscher D, Schett G, Strangfeld A, Zink A (2016) Body mass index distribution in rheumatoid arthritis: a collaborative analysis from three large German rheumatoid arthritis databases. Arthritis Res Ther 18:149
Du T, Sun X, Yin P, Huo R, Ni C, Yu X (2013) Increasing trends in central obesity among Chinese adults with normal body mass index, 1993-2009. BMC Public Health 13:327
Kahn HS, Bullard KM (2016) Beyond body mass index: advantages of abdominal measurements for recognizing cardiometabolic disorders. Am J Med 129:74–81.e2
Savva SC, Lamnisos D, Kafatos AG (2013) Predicting cardiometabolic risk: waist-to-height ratio or BMI. A meta-analysis. Diabetes Metab Syndr Obes 6:403–419
Little RR, Roberts WL (2009) A review of variant hemoglobins interfering with hemoglobin A1c measurement. J Diabetes Sci Technol 3:446–451
Kellner H, Bornholdt K, Hein G (2010) Leflunomide in the treatment of patients with early rheumatoid arthritis—results of a prospective non-interventional study. Clin Rheumatol 29:913–920
Protogerou AD, Panagiotakos DB, Zampeli E, Argyris AA, Arida K, Konstantonis GD, Pitsavos C, Kitas GD, Sfikakis PP (2013) Arterial hypertension assessed “out-of-office” in a contemporary cohort of rheumatoid arthritis patients free of cardiovascular disease is characterized by high prevalence, low awareness, poor control and increased vascular damage-associated “white coat” phenomenon. Arthritis Res Ther 15:R142
Boers M, Nurmohamed MT, Doelman CJ, Lard LR, Verhoeven AC, Voskuyl AE, Huizinga TW, van de Stadt RJ, Dijkmans BA, van der Linden S (2003) Influence of glucocorticoids and disease activity on total and high density lipoprotein cholesterol in patients with rheumatoid arthritis. Ann Rheum Dis 62:842–845
Nurmohamed MT, Heslinga M, Kitas GD (2015) Cardiovascular comorbidity in rheumatic diseases. Nat Rev Rheumatol 11:693–704
Toms TE, Panoulas VF, Douglas KM, Nightingale P, Smith JP, Griffiths H, Sattar N, Symmons DP, Kitas GD (2011) Are lipid ratios less susceptible to change with systemic inflammation than individual lipid components in patients with rheumatoid arthritis? Angiology 62:167–175
Pérez de Isla L; SEC Working Group for the 2016 ESC Guidelines for the Management of Dyslipidemias:, Pérez de Isla L, Fernández PL, Álvarez-Sala Walther L, Barrios Alonso V, Castro Conde A, Galve Basilio E, García Ortiz L, Mata López P; Expert Reviewers for the 2016 ESC Guidelines for the Management of Dyslipidemias:, Alegría Ezquerra E, Cordero Fort A, Cosin Sales J, Escobar Cervantes C, García-Moll Marimón X, José Gómez Doblas J, Marzal Martín D, Murga Eizagaechevarria N, de Pablo Zarzosa C, Miguel Rincón L, Sanchis Forés J; SEC Guidelines Committee:, Alberto San Román Calvar J, Alfonso Manterola F, Arribas Ynsaurriaga F, Evangelista Masip A, Ferreira González I, Jiménez Navarro M, Marín Ortuño F, Pérez de Isla L, Rodríguez Padial L, Luis Sánchez Fernández P, Sionis Green A, Vázquez García R (2017) Comments on the 2016 ESC/EAS Guidelines for the Management of Dyslipidemias. Rev Esp Cardiol (Engl Ed) 70:72–77
van den Oever IAM, Heslinga M, Griep EN, Griep-Wentink HRM, Schotsman R, Cambach W, Dijkmans BAC, Smulders YM, Lems WF, Boers M, Voskuyl EA, Peters MJL, van Schaardenburg D, Nurmohamed MT (2017) Cardiovascular risk management in rheumatoid arthritis patients still suboptimal: the Implementation of Cardiovascular Risk Management in Rheumatoid Arthritis project. Rheumatology
Crowson CS, Matteson EL, Roger VL, Therneau TM, Gabriel SE (2012) Usefulness of Risk Scores to Estimate the Risk of Cardiovascular Disease in Patients With Rheumatoid Arthritis. The American Journal of Cardiology 110(3):420–424
Arts EEA, Popa C, Den Broeder AA, Semb AG, Toms T, Kitas GD, van Riel PL, Fransen J (2015) Performance of four current risk algorithms in predicting cardiovascular events in patients with early rheumatoid arthritis. Annals of the Rheumatic Diseases 74(4):668–674
Acknowledgements
The authors thank all the colleagues of laboratory in Hangzhou Sanatorium of People’s Liberation Army.
Funding
This study was supported by National Natural Science Foundation of China (No. 81671595 and 81471607).
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This study was a retrospective study; clinical data collection of patients was approved by the Ethics Committee of the Shanghai Changhai Hospital.
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Liu, X.Z., Gao, Y., Fan, J. et al. Metabolic abnormalities in rheumatoid arthritis patients with comorbid diabetes mellitus. Clin Rheumatol 37, 219–226 (2018). https://doi.org/10.1007/s10067-017-3847-7
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DOI: https://doi.org/10.1007/s10067-017-3847-7