The effects of tumor necrosis factor inhibitors on cardiovascular risk in rheumatoid arthritis

Current Pharmaceutical Design

Volumn 18, Issue 11, 2012, Pages 1502-1511

  Peters, Mike J L ^a   van Sijl, Alper M ^a,b,c   Voskuyl, Alexandre E ^c   Sattar, Naveed ^d   Smulders, Yvo M ^a   Nurmohamed, Michael T ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Reade   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Cardiovascular disease; Inflammation; Rheumatoid arthritis; TNF inhibitors

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL; NITRIC OXIDE; TUMOR NECROSIS FACTOR INHIBITOR;

ARTERIAL WALL THICKNESS; BLOOD CLOTTING; CACHEXIA; CARDIOVASCULAR DISEASE; CARDIOVASCULAR PROCEDURES; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; DIABETES MELLITUS; DISEASE ASSOCIATION; DRUG EFFECT; DYSLIPIDEMIA; ENDOTHELIAL DYSFUNCTION; FLOW MEDIATED DILATION; HUMAN; HYPERTENSION; INFLAMMATION; INSULIN RESISTANCE; NON INVASIVE MEASUREMENT; PRIORITY JOURNAL; PULSE WAVE; REVIEW; RHEUMATOID ARTHRITIS; RISK MANAGEMENT; RISK REDUCTION; SYSTEMATIC REVIEW; SYSTOLIC BLOOD PRESSURE; VASCULAR ENDOTHELIUM; VASODILATATION;

EID: 84857732549     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161212799504786     Document Type: Review

References (117)

1. Lawrence RC, Helmick CG, Arnett FC, et al. Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States. Arthritis Rheum 1998; 41: 778-799.
2. [DP. Epidemiology of rheumatoid arthritis: determinants of onset, persistence and outcome. Best Pract Res Clin Rheumatol 2002; 16: 707-722.
3. Van Doornum S, McColl G, Wicks IP. Accelerated atherosclerosis: an extraarticular feature of rheumatoid arthritis? Arthritis Rheum 2002; 46: 862-873.
4. Meune C, Touze E, Trinquart L, Allanore Y. Trends in cardiovascular mortality in patients with rheumatoid arthritis over 50 years: a systematic review and meta-analysis of cohort studies. Rheumatology (Oxford) 2009; 48: 1309-1313.
5. van Halm VP, Peters MJ, Voskuyl AE, et al. Rheumatoid arthritis versus diabetes as a risk factor for cardiovascular disease, a cross sectional study. The CARRE Investigation. Ann Rheum Dis 2009; 68(9): 1395-1400.
6. Lindhardsen J, Ahlehoff O, Gislason GH, et al. The risk of myocardial infarction in rheumatoid arthritis and diabetes mellitus: a Danish nationwide cohort study. Ann Rheum Dis 2011; 70(6): 929-934.
7. del Rincon ID, Williams K, Stern MP, Freeman GL, Escalante A. High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum 2001; 44: 2737-2745.
8. Solomon DH, Karlson EW, Rimm EB, et al. Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 2003; 107: 1303-130y7.
9. Solomon DH, Kremer J, Curtis JR, et al. Explaining the cardiovascular risk associated with rheumatoid arthritis: traditional risk factors versus markers of rheumatoid arthritis severity. Ann Rheum Dis 2010; 69(11): 1920-5.
10. Sattar N, McCarey DW, Capell H, McInnes IB. Explaining how high-grade systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation 2003; 108: 2957-63.
11. Esposito E, Cuzzocrea S. TNF-alpha as a therapeutic target in in flammatory diseases, ischemia-reperfusion injury and trauma. Curr Med Chem 2009; 16: 3152-67.
12. Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-74.
13. Scott DL, Kingsley GH. Tumor necrosis factor inhibitors for rheumatoid arthritis. N Engl J Med 2006; 355: 704-12.
14. Wong M, Ziring D, Korin Y, et al. TNFalpha blockade in human diseases: mechanisms and future directions. Clin Immunol 2008; 126: 121-36.
15. Papadakis KA, Targan SR. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med 2000; 51: 289-98.
16. Scallon BJ, Moore MA, Trinh H, Knight DM, Ghrayeb J. Chimeric anti-TNF-alpha monoclonal antibody cA2 binds recombinant transmembrane TNF-alpha and activates immune effector functions. Cytokine 1995; 7: 251-9.
17. Mitoma H, Horiuchi T, Hatta N, et al. Infliximab induces potent anti-inflammatory responses by outside-to-inside signals through transmembrane TNF-alpha. Gastroenterology 2005; 128: 376-92.
18. Charles P, Elliott MJ, Davis D, et al. Regulation of cytokines, cyto-kine inhibitors, and acute-phase proteins following anti-TNF-alpha therapy in rheumatoid arthritis. J Immunol 1999; 163: 1521-8.
19. Taylor PC, Peters AM, Paleolog E, et al. Reduction of chemokine levels and leukocyte traffic to joints by tumor necrosis factor alpha blockade in patients with rheumatoid arthritis. Arthritis Rheum 2000; 43: 38-47.
20. Paleolog EM, Young S, Stark AC, McCloskey RV, Feldmann M, Maini RN. Modulation of angiogenic vascular endothelial growth factor by tumor necrosis factor alpha and interleukin-1 in rheumatoid arthritis. Arthritis Rheum 1998; 41: 1258-65.
21. Klimiuk PA, Sierakowski S, Domyslawska I, Fiedorczyk M, Chwiecko J. Reduction of soluble adhesion molecules (sICAM-1, sVCAM-1, and sE-selectin) and vascular endothelial growth factor levels in serum of rheumatoid arthritis patients following multiple intravenous infusions of infliximab. Arch Immunol Ther Exp (Warsz) 2004; 52: 36-42.
22. Jacobsson LT, Turesson C, Gulfe A, et al. Treatment with tumor necrosis factor blockers is associated with a lower incidence of first cardiovascular events in patients with rheumatoid arthritis. J Rheu-matol 2005; 32: 1213-8.
23. Carmona L, Descalzo MA, Perez-Pampin E, et al. All-cause and cause-specific mortality in rheumatoid arthritis are not greater than expected when treated with tumour necrosis factor antagonists. Ann Rheum Dis 2007; 66: 880-885.
24. Greenberg JD, Kremer JM, Curtis JR, et al. Tumour necrosis factor antagonist use and associated risk reduction of cardiovascular events among patients with rheumatoid arthritis. Ann Rheum Dis 2011 70(4): 576-82.
25. Lunt M, Watson KD, Dixon WG, Symmons DP, Hyrich KL. No evidence of association between anti-TNF treatment and mortality in patients with rheumatoid arthritis: Results from the British Society for Rheumatology Biologics Register. Arthritis Rheum 2010; 62(11): 3145-53.
26. Solomon DH, Avorn J, Katz JN, et al. Immunosuppressive medications and hospitalization for cardiovascular events in patients with rheumatoid arthritis. Arthritis Rheum 2006; 54: 3790-8.
27. Hochberg MC, Johnston SS, John AK. The incidence and prevalence of extra-articular and systemic manifestations in a cohort of newly-diagnosed patients with rheumatoid arthritis between 1999 and 2006. Curr Med Res Opin 2008; 24: 469-80.
28. Dixon WG, Watson KD, Lunt M, Hyrich KL, Silman AJ, Symmons DPM. Reduction in the incidence of myocardial infarction in patients with rheumatoid arthritis who respond to anti-tumor necrosis factor alpha therapy: results from the British Society for Rheumatology Biologics Register. Arthritis Rheum 2007; 56: 2905-12.
29. Naranjo A, Sokka T, Descalzo MA, et al. Cardiovascular disease in patients with rheumatoid arthritis: results from the QUEST-RA study. Arthritis Res Ther 2008; 10: R30.
30. Al Aly Z, Pan H, Zeringue A, et al. Tumor necrosis factor-alpha blockade, cardiovascular outcomes, and survival in rheumatoid arthritis. Transl Res 2011; 157: 10-18.
31. Suissa S, Bernatsky S, Hudson M. Antirheumatic drug use and the risk of acute myocardial infarction. Arthritis Rheum 2006; 55: 531-6.
32. Nadareishvili Z, Michaud K, Hallenbeck JM, Wolfe F. Cardiovascular, rheumatologic, and pharmacologic predictors of stroke in patients with rheumatoid arthritis: a nested, case-control study. Arthritis Rheum 2008; 59: 1090-6.
33. Wolfe F, Michaud K. The risk of myocardial infarction and phar-macologic and nonpharmacologic myocardial infarction predictors in rheumatoid arthritis: A cohort and nested case-control analysis. Arthritis Rheum 2008; 58: 2612-21.
34. Barnabe C, Martin BJ, Ghali WA. Systematic review and meta-analysis: Anti-tumor necrosis factor alpha therapy and cardiovascular events in rheumatoid arthritis. Arthritis Care Res (Hoboken) 2011; 63(4): 522-9.
35. van Sijl AM, Peters MJ, Knol DK, et al. Carotid Intima Media Thickness in Rheumatoid Arthritis as Compared to Control Subjects: A Meta-Analysis. Semin Arthritis Rheum 2011; 40(5): 389-97.
36. Maki-Petaja KM, Hall FC, Booth AD, et al. Rheumatoid arthritis is associated with increased aortic pulse-wave velocity, which is reduced by anti-tumor necrosis factor-alpha therapy. Circulation 2006; 114: 1185-92.
37. Khan F, Galarraga B, Belch JJ. The role of endothelial function and its assessment in rheumatoid arthritis. Nat Rev Rheumatol 2010; 6: 253-61.
38. Sandoo A, Veldhuijzen van Zanten JJ, Metsios GS, Carroll D, Kitas GD. Vascular function and morphology in rheumatoid arthritis: a systematic review. Rheumatology (Oxford) 2011; 50: 2125-39.
39. Danesh J, Wheeler JG, Hirschfield GM, et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N Engl J Med 2004; 350: 1387-97.
40. Lombardo A, Biasucci LM, Lanza GA, et al. Inflammation as a possible link between coronary and carotid plaque instability. Circulation 2004; 109: 3158-63.
41. Sattar N, Lowe GD. High sensitivity C-reactive protein and cardiovascular disease: an association built on unstable foundations? Ann Clin Biochem 2006; 43: 252-6.
42. Aubry MC, Maradit-Kremers H, Reinalda MS, Crowson CS, Edwards WD, Gabriel SE. Differences in atherosclerotic coronary heart disease between subjects with and without rheumatoid arthritis. J Rheumatol 2007; 34: 937-42.
43. Sattar N, Murray HM, Welsh P, Blauw GJ, Buckley BM, Cobbe S et al. Are markers of inflammation more strongly associated with risk for fatal than for nonfatal vascular events? PLoS Med 2009; 6: e1000099.
44. Van Doornum S, Brand C, King B, Sundararajan V. Increased case fatality rates following a first acute cardiovascular event in patients with rheumatoid arthritis. Arthritis Rheum 2006; 54: 2061-8.
45. Maradit-Kremers H, Crowson CS, Nicola PJ, et al. Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum 2005; 52: 402-11.
46. Choy E, Sattar N. Interpreting lipid levels in the context of high-grade inflammatory states with a focus on rheumatoid arthritis: a challenge to conventional cardiovascular risk actions. Ann Rheum Dis 2009; 68: 460-9.
47. van Sijl AM, Peters MJ, Knol DL, et al. The effect of TNF-alpha blocking therapy on lipid levels in rheumatoid arthritis: a meta-analysis. Semin Arthritis Rheum 2011; 41: 393-400.
48. Hahn BH, Grossman J, Ansell BJ, Skaggs BJ, McMahon M. Altered lipoprotein metabolism in chronic inflammatory states: proin-flammatory high-density lipoprotein and accelerated atherosclerosis in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Res Ther 2008; 10: 213.
49. van Eijk IC, de Vries MK, Levels JH, et al. Improvement of lipid profile is accompanied by atheroprotective alterations in high-density lipoprotein composition upon tumor necrosis factor blockade: A prospective cohort study in ankylosing spondylitis. Arthritis Rheum 2009; 60: 1324-30.
50. Kannel WB. Blood pressure as a cardiovascular risk factor: prevention and treatment. JAMA 1996; 275: 1571-6.
51. Gonzalez A, Maradit KH, Crowson CS, et al. Do cardiovascular risk factors confer the same risk for cardiovascular outcomes in rheumatoid arthritis patients as in non-RA patients? Ann Rheum Dis 2007; 67(1): 64-9.
52. Abramson JL, Weintraub WS, Vaccarino V. Association between pulse pressure and C-reactive protein among apparently healthy US adults. Hypertension 2002; 39: 197-202.
53. Wong M, Toh L, Wilson A, et al. Reduced arterial elasticity in rheumatoid arthritis and the relationship to vascular disease risk factors and inflammation. Arthritis Rheum 2003; 48: 81-9.
54. de Groot L, Posthumus MD, Kallenberg CG, Bijl M. Risk factors and early detection of atherosclerosis in rheumatoid arthritis. Eur J Clin Invest 2010; 40(9): 835-42.
55. van den Oever IAM, Raterman HG, Nurmohamed MT, Simsek S. Endothelial dysfunction, inflammation, and apoptosis in diabetes mellitus. Mediators Inflamm 2010; 2010: 792393.
56. Datta D, Ferrell WR, Sturrock RD, Jadhav ST, Sattar N. Inflammatory suppression rapidly attenuates microvascular dysfunction in rheumatoid arthritis. Atherosclerosis 2007; 192: 391-5.
57. Protogerou AD, Zampeli E, Fragiadaki K, Stamatelopoulos K, Papamichael C, Sfikakis PP. A pilot study of endothelial dysfunction and aortic stiffness after interleukin-6 receptor inhibition in rheumatoid arthritis. Atherosclerosis 2011; 219: 734-6.
58. Wong M, Oakley SP, Young L, et al. Infliximab improves vascular stiffness in patients with rheumatoid arthritis. Ann Rheum Dis 2009; 68: 1277-84.
59. Angel K, Provan SA, Gulseth HL, Mowinckel P, Kvien TK, Atar D. Tumor necrosis factor-alpha antagonists improve aortic stiffness in patients with inflammatory arthropathies: a controlled study. Hypertension 2010; 55: 333-8.
60. Komai N, Morita Y, Sakuta T, Kuwabara A, Kashihara N. Anti-tumor necrosis factor therapy increases serum adiponectin levels with the improvement of endothelial dysfunction in patients with rheumatoid arthritis. Mod Rheumatol 2007; 17: 385-90.
61. Kerekes G, Soltesz P, Szucs G, et al. Effects of adalimumab treatment on vascular disease associated with early rheumatoid arthritis. Isr Med Assoc J 2011; 13: 147-52.
62. Mazzoccoli G, Notarsanto I, de Pinto GD, et al. Anti-tumor necrosis factor-alpha therapy and changes of flow-mediated vasodilata-tion in psoriatic and rheumatoid arthritis patients. Intern Emerg Med 2010; 5(6): 495-500.
63. Sidiropoulos PI, Siakka P, Pagonidis K, et al. Sustained improvement of vascular endothelial function during anti-TNFalpha treatment in rheumatoid arthritis patients. Scand J Rheumatol 2009; 38: 6-10.
64. Gonzalez-Juanatey C, Testa A, Garcia-Castelo A, Garcia-Porrua C, Llorca J, Gonzalez-Gay MA. Active but transient improvement of endothelial function in rheumatoid arthritis patients undergoing long-term treatment with anti-tumor necrosis factor alpha antibody. Arthritis Rheum 2004; 51: 447-450.
65. Hurlimann D, Forster A, Noll G, et al. Anti-tumor necrosis factor-alpha treatment improves endothelial function in patients with rheumatoid arthritis. Circulation 2002; 106: 2184-7.
66. Irace C, Mancuso G, Fiaschi E, Madia A, Sesti G, Gnasso A. Effect of anti TNFalpha therapy on arterial diameter and wall shear stress and HDL cholesterol. Atherosclerosis 2004; 177: 113-8.
67. Bilsborough W, Keen H, Taylor A, O'Driscoll GJ, Arnolda L, Green DJ. Anti-tumour necrosis factor-alpha therapy over conventional therapy improves endothelial function in adults with rheumatoid arthritis. Rheumatol Int 2006; 26: 1125-31.
68. Bosello S, Santoliquido A, Zoli A, et al. TNF-alpha blockade induces a reversible but transient effect on endothelial dysfunction in patients with long-standing severe rheumatoid arthritis. Clin Rheu-matol 2008; 27: 833-9.
69. Tikiz H, Arslan O, Pirildar T, Tikiz C, Bayindir P. The effect of anti-tumor necrosis factor (TNF)-alpha therapy with etanercept on endothelial functions in patients with rheumatoid arthritis. Anadolu Kardiyol Derg 2010; 10: 98-103.
70. Gonzalez-Juanatey C, Llorca J, Garcia-Porrua C, Martin J, Gonzalez-Gay MA. Effect of anti-tumor necrosis factor alpha therapy on the progression of subclinical atherosclerosis in severe rheumatoid arthritis. Arthritis Rheum 2006; 55: 150-3.
71. Klarenbeek NB, van der Kooij SM, Huizinga TJ, et al. Blood pressure changes in patients with recent-onset rheumatoid arthritis treated with four different treatment strategies: a post hoc analysis from the BeSt trial. Ann Rheum Dis 2010; 69: 1342-5.
72. Yudkin JS, Stehouwer CD, Emeis JJ, Coppack SW. C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 1999; 19: 972-8.
73. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993; 259: 87-91.
74. [GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 1996; 271: 665-8.
75. Svenson KL, Pollare T, Lithell H, Hallgren R. Impaired glucose handling in active rheumatoid arthritis: relationship to peripheral insulin resistance. Metabolism 1988; 37: 125-30.
76. Dessein PH, Joffe BI. Insulin resistance and impaired beta cell function in rheumatoid arthritis. Arthritis Rheum 2006; 54: 2765-75.
77. Chung CP, Oeser A, Solus JF, et al. Inflammation-associated insulin resistance: differential effects in rheumatoid arthritis and systemic lupus erythematosus define potential mechanisms. Arthritis Rheum 2008; 58: 2105-12.
78. Pagano G, Bruno A, Cavallo-Perin P, Cesco L, Imbimbo B. Glucose intolerance after short-term administration of corticosteroids in healthy subjects. Prednisone, deflazacort, and betamethasone. Arch Intern Med 1989; 149: 1098-101.
79. Stavropoulos-Kalinoglou A, Metsios GS, Panoulas VF, et al. Associations of obesity with modifiable risk factors for the development of cardiovascular disease in patients with rheumatoid arthritis. Ann Rheum Dis 2009; 68: 242-5.
80. Doran M. Rheumatoid arthritis and diabetes mellitus: evidence for an association? J Rheumatol 2007; 34: 460-2.
81. Wasko MC, Kay J, Hsia EC, Rahman MU. Diabetes mellitus and insulin resistance in patients with rheumatoid arthritis: Risk reduction in a chronic inflammatory disease. Arthritis Care Res (Hoboken) 2011; 63: 512-21.
82. Sattar N, Nelson SM. Adiponectin, diabetes, and coronary heart disease in older persons: unraveling the paradox. J Clin Endocrinol Metab 2008; 93: 3299-301.
83. Fantuzzi G. Adiponectin and inflammation: consensus and controversy. J Allergy Clin Immunol 2008; 121: 326-30.
84. Gonzalez-Gay MA, de Matias JM, 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.
85. Tam LS, Tomlinson B, Chu TT, Li TK, Li EK. Impact of TNF inhibition on insulin resistance and lipids levels in patients with rheumatoid arthritis. Clin Rheumatol 2007; 26: 1495-8.
86. Rosenvinge A, Krogh-Madsen R, Baslund B, Pedersen BK. Insulin resistance in patients with rheumatoid arthritis: effect of anti-TNFalpha therapy. Scand J Rheumatol 2007; 36: 91-6.
87. Kiortsis DN, Mavridis AK, Vasakos S, Nikas SN, Drosos AA. Effects of infliximab treatment on insulin resistance in patients with rheumatoid arthritis and ankylosing spondylitis. Ann Rheum Dis 2005; 64: 765-6.
88. van Eijk IC, Peters MJL, Nurmohamed MT, van Deutekom AW, Dijkmans BAC, Simsek S. Decrease of fructosamine levels during treatment with adalimumab in patients with both diabetes and rheumatoid arthritis. Eur J Endocrinol 2007; 156: 291-3.
89. 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: 2525-31.
90. Elkind MS, Carty CL, O'Meara ES, et al. Hospitalization for infection and risk of acute ischemic stroke: the Cardiovascular Health Study. Stroke 2011; 42: 1851-6.
91. Gasparyan AY, Stavropoulos-Kalinoglou A, Mikhailidis DP, Douglas KM, Kitas GD. Platelet function in rheumatoid arthritis: arthritic and cardiovascular implications. Rheumatol Int 2011; 31: 153-64.
92. Levi M, van der PT, Buller HR. Bidirectional relation between inflammation and coagulation. Circulation 2004; 109: 2698-704.
93. Borissoff JI, Spronk HM, Ten Cate H. The hemostatic system as a modulator of atherosclerosis. N Engl J Med 2011; 364: 1746-60.
94. Gasparyan AY, Sandoo A, Stavropoulos-Kalinoglou A, Kitas GD. Mean platelet volume in patients with rheumatoid arthritis: the effect of anti-TNF-a therapy. Rheumatol Int 2010; 30: 1125-9.
95. Ingegnoli F, Fantini F, Favalli EG, et al. Inflammatory and prothrombotic biomarkers in patients with rheumatoid arthritis: ef-fects of tumor necrosis factor-alpha blockade. J Autoimmun 2008; 31: 175-9.
96. Agirbasli M, Inanc N, Baykan OA, Direskeneli H. The effects of TNF alpha inhibition on plasma fibrinolytic balance in patients with chronic inflammatory rheumatical disorders. Clin Exp Rheumatol 2006; 24: 580-3.
97. Summers GD, Metsios GS, Stavropoulos-Kalinoglou A, Kitas GD. Rheumatoid cachexia and cardiovascular disease. Nat Rev Rheuma-tol 2010; 6: 445-51.
98. Elkan AC, Hakansson N, Frostegard J, Cederholm T, Hafstrom I. Rheumatoid cachexia is associated with dyslipidemia and low levels of atheroprotective natural antibodies against phosphorylcholine but not with dietary fat in patients with rheumatoid arthritis: a cross-sectional study. Arthritis Res Ther 2009; 11: R37.
99. Metsios GS, Stavropoulos-Kalinoglou A, Panoulas VF, et al. Rheumatoid cachexia and cardiovascular disease. Clin Exp Rheu-matol 2009; 27: 985-8.
100. Engvall IL, Elkan AC, Tengstrand B, Cederholm T, Brismar K, Hafstrom I. Cachexia in rheumatoid arthritis is associated with inflammatory activity, physical disability, and low bioavailable insulin-like growth factor. Scand J Rheumatol 2008; 37: 321-8.
101. Roubenoff R, Roubenoff RA, Ward LM, Holland SM, Hellmann DB. Rheumatoid cachexia: depletion of lean body mass in rheumatoid arthritis. Possible association with tumor necrosis factor. J Rheumatol 1992; 19: 1505-10.
102. Munro R, Capell H. Prevalence of low body mass in rheumatoid arthritis: association with the acute phase response. Ann Rheum Dis 1997; 56: 326-9.
103. Kremers HM, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE. Prognostic importance of low body mass index in relation to cardiovascular mortality in rheumatoid arthritis. Arthritis Rheum 2004; 50: 3450-7.
104. Kitas GD, Gabriel SE. Cardiovascular disease in rheumatoid arthritis: state of the art and future perspectives. Ann Rheum Dis 2011; 70: 8-14.
105. Summers GD, Deighton CM, Rennie MJ, Booth AH. Rheumatoid cachexia: a clinical perspective. Rheumatology (Oxford) 2008; 47: 1124-31.
106. Marcora SM, Chester KR, Mittal G, Lemmey AB, Maddison PJ. Randomized phase 2 trial of anti-tumor necrosis factor therapy for cachexia in patients with early rheumatoid arthritis. Am J Clin Nutr 2006; 84: 1463-72.
107. Petri H, Urquhart J. Channeling bias in the interpretation of drug effects. Stat Med 1991; 10: 577-81.
108. Gregg EW, Gu Q, Cheng YJ, Narayan KM, Cowie CC. Mortality trends in men and women with diabetes, 1971 to 2000. Ann Intern Med 2007; 147: 149-55.
109. Fox CS, Coady S, Sorlie PD, et al. Trends in cardiovascular complications of diabetes. JAMA 2004; 292: 2495-9.
110. Seshasai SR, Kaptoge S, Thompson A, et al. Diabetes mellitus, fasting glucose, and risk of cause-specific death. N Engl J Med 2011; 364: 829-41.
111. Conroy RM, Pyorala K, Fitzgerald AP, et al. Estimation of ten-year risk of fatal cardiovascular disease in Europe: the SCORE project. Eur Heart J 2003; 24: 987-1003.
112. Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998; 97: 1837-47.
113. Smulders YM, Spijkerman AM, Kostense PJ, Bouter LM, Stehou-wer CD. [Old and new scoring systems for assessing cardiovascular risks: problems with the validity, the precision and the homogenic-ity of the risk categories]. Ned Tijdschr Geneeskd 2004; 148: 2480-4.
114. Peters MJL, Symmons DPM, McCarey D, et al. EULAR evidence-based recommendations for cardiovascular risk management in patients with rheumatoid arthritis and other forms of inflammatory arthritis. Ann Rheum Dis 2010; 69: 325-31.
115. Del Porto F, Lagana B, Lai S, et al. Response to anti-tumour necrosis factor alpha blockade is associated with reduction of carotid in-tima-media thickness in patients with active rheumatoid arthritis. Rheumatology (Oxford) 2007; 46: 1111-5.
116. Di Micco P, Ferrazzi P, Libre L, et al. Intima-media thickness evolution after treatment with infliximab in patients with rheumatoid arthritis. Int J Gen Med 2009; 2: 141-4.
117. Turiel M, Atzeni F, Tomasoni L, et al. Non-invasive assessment of coronary flow reserve and ADMA levels: a case-control study of early rheumatoid arthritis patients. Rheumatology (Oxford) 2009; 48: 834-9.