Lipid profile changes in patients with rheumatic diseases receiving a treatment with TNF-α blockers: A meta-analysis of prospective studies

References

• Di Minno MN, Iervolino S, Lupoli R, Russolillo A, Coppola A, Peluso R, et al. Cardiovascular risk in rheumatic patients: the link between inflammation and atherothrombosis. Semin Thromb Hemost. 2012;38:497–505.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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;44:2737–45.
   PubMed Web of Science ®Google Scholar
• van Kuijk AW, Reinders-Blankert P, Smeets TJ, Dijkmans BA, Tak PP. Detailed analysis of the cell infiltrate and the expression of mediators of synovial inflammation and joint destruction in the synovium of patients with psoriatic arthritis: implications for treatment. Ann Rheum Dis. 2006;65:1551–7.
   PubMed Web of Science ®Google Scholar
• Dixon WG, Symmons DP. What effects might anti-TNF-α treatment be expected to have on cardiovascular morbidity and mortality in rheumatoid arthritis? A review of the role of TNF-alpha in cardiovascular pathophysiology. Ann Rheum Dis. 2007;66:1132–6.
   PubMed Web of Science ®Google Scholar
• Popa C, van den Hoogen FH, Radstake TR, Netea MG, Eijsbouts AE, den Heijer M, et al. Modulation of lipoprotein plasma concentrations during long-term anti-TNF-α therapy in patients with active rheumatoid arthritis. Ann Rheum Dis. 2007;66:1503–7.
   PubMed Web of Science ®Google Scholar
• Libby P. Changing concepts of atherogenesis. J Intern Med. 2000;247: 349–58.
   PubMed Web of Science ®Google Scholar
• Mazzoccoli G, Notarsanto I, de Pinto GD, Dagostino MP, De Cata A, D’Alessandro G, et al. Anti-tumor necrosis factor-α therapy and changes of flow-mediated vasodilatation in psoriatic and rheumatoid arthritis patients. Intern Emerg Med. 2010;5:495–500.
   PubMed Web of Science ®Google Scholar
• Tam LS, Li EK, Shang Q, Tomlinson B, Li M, Leung YY, et al. Tumour necrosis factor alpha blockade is associated with sustained regression of carotid intima-media thickness for patients with active psoriatic arthritis: a 2-year pilot study. Ann Rheum Dis. 2011; 70:705–6.
   PubMedGoogle Scholar
• Peters MJ, Symmons DP, McCarey D, Dijkmans BA, Nicola P, Kvien TK, 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.
   PubMed Web of Science ®Google Scholar
• Di Minno MN, Iervolino S, Peluso R, Scarpa R, Di Minno G. Platelet reactivity and disease activity in subjects with psoriatic arthritis. J Rheumatol. 2012;39:334–6.
   PubMed Web of Science ®Google Scholar
• Mac Mullan PA, Peace AJ, Madigan AM, Tedesco AF, Kenny D, McCarthy GM. Platelet hyper-reactivity in active inflammatory arthritis is unique to the adenosine diphosphate pathway: a novel finding and potential therapeutic target. Rheumatology (Oxford). 2010;49:240–5.
   PubMed Web of Science ®Google Scholar
• Pamuk GE, Vural O, Turgut B, Demir M, Pamuk ON, Cakir N. Increased platelet activation markers in rheumatoid arthritis: are they related with subclinical atherosclerosis?Platelets. 2008;19:146–54.
   PubMed Web of Science ®Google Scholar
• Di Minno MN, Peluso R, Iervolino S, Lupoli R, Russolillo A, Tarantino G, et al. Hepatic steatosis, carotid plaques and achieving MDA in psoriatic arthritis patients starting TNF-α blockers treatment: a prospective study. Arthritis Res Ther. 2012;14:R211.
   PubMedGoogle Scholar
• Gonzalez-Juanatey C, Vazquez-Rodriguez TR, Miranda-Filloy JA, Gomez-Acebo I, Testa A, Garcia-Porrua C, et al. Anti-TNF-α- adalimumab therapy is associated with persistent improvement of endothelial function without progression of carotid intima-media wall thickness in patients with rheumatoid arthritis refractory to conventional therapy. Mediators Inflamm. 2012;2012:674265.
   PubMed Web of Science ®Google Scholar
• Di Minno MN, Iervolino S, Peluso R, Scarpa R, Di Minno G; CaRRDs Study Group. Carotid intima-media thickness in psoriatic arthritis: differences between tumor necrosis factor-α blockers and traditional disease-modifying antirheumatic drugs. Arterioscler Thromb Vasc Biol. 2011;31:705–12.
   PubMed Web of Science ®Google Scholar
• Di Minno MN, Iervolino S, Peluso R, Russolillo A, Lupoli R, Scarpa R, et al. Hepatic steatosis and disease activity in subjects with psoriatic arthritis receiving tumor necrosis factor-α blockers. J Rheumatol. 2012;39:1042–6.
   PubMed Web of Science ®Google Scholar
• Del Porto F, Laganà B, Lai S, Nofroni I, Tinti F, Vitale M, et al. Response to anti-tumour necrosis factor alpha blockade is associated with reduction of carotid intima-media thickness in patients with active rheumatoid arthritis. Rheumatology (Oxford). 2007;46:1111–15.
   PubMed Web of Science ®Google Scholar
• Channual J, Wu JJ, Dann FJ. Effects of tumor necrosis factor-α blockade on metabolic syndrome components in psoriasis and psoriatic arthritis and additional lessons learned from rheumatoid arthritis. Dermatol Ther. 2009;22:61–73.
   PubMed Web of Science ®Google Scholar
• Miranda-Filloy JA, Llorca J, Carnero-López B, González-Juanatey C, Blanco R, González-Gay MA. TNF-alpha antagonist therapy improves insulin sensitivity in non-diabetic ankylosing spondylitis patients. Clin Exp Rheumatol. 2012;30:850–5.
   PubMed Web of Science ®Google Scholar
• Stagakis I, Bertsias G, Karvounaris S, Kavousanaki M, Virla D, Raptopoulou A, et al. Anti-tumor necrosis factor therapy improves insulin resistance, beta cell function and insulin signaling in active rheumatoid arthritis patients with high insulin resistance. Arthritis Res Ther. 2012;14:R141.
   PubMed Web of Science ®Google Scholar
• Popa CD, Arts E, Fransen J, van Riel PL. Atherogenic index and high-density lipoprotein cholesterol as cardiovascular risk determinants in rheumatoid arthritis: the impact of therapy with biologicals. Mediators Inflamm. 2012;2012:785946.
   PubMed Web of Science ®Google Scholar
• Schimmel EK, Yazici Y. Increased lipid levels but unchanged atherogenic index in rheumatoid arthritis patients treated with biologic disease modifying antirheumatic drugs: published experience. Clin Exp Rheumatol. 2009;27:446–51.
   PubMed Web of Science ®Google Scholar
• Wells G, Shea B. Data extraction for nonrandomised systematic reviews. University of Ottowa, Ottowa. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm (accessed on 5 November 2013).
   Google Scholar
• Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.
   PubMed Web of Science ®Google Scholar
• Sterne JA, Egger M, Smith GD. Systematic reviews in health care: investigating and dealing with publication and other biases in meta-analysis. BMJ. 2001;323:101–5.
   PubMed Web of Science ®Google Scholar
• Seriolo B, Paolino S, Ferrone C, Cutolo M. Effects of etanercept or infliximab treatment on lipid profile and insulin resistance in patients with refractory rheumatoid arthritis. Clin Rheumatol. 2007;26:1799–800.
   PubMedGoogle Scholar
• Seriolo B, Paoliono S, Ferrone C, Cutolo M. Comments on the original article by Soubrier et al. Effects of anti-tumor necrosis factor therapy on lipid profile in patients with rheumatoid arthritis. Joint Bone Spine. 2009;76:117–18.
   Google Scholar
• Seriolo B, Paolino S, Sulli A, Fasciolo D, Cutolo M. Effects of anti-TNF-α treatment on lipid profile in patients with active rheumatoid arthritis. Ann N Y Acad Sci. 2006;1069:414–19.
   PubMed Web of Science ®Google Scholar
• Cauza E, Cauza K, Hanusch-Enserer U, Etemad M, Dunky A, Kostner K. Intravenous anti TNF-alpha antibody therapy leads to elevated triglyceride and reduced HDLc-cholesterol levels in patients with rheumatoid and psoriatic arthritis. Wien Klin Wochenschr. 2002; 114:1004–7.
   PubMed Web of Science ®Google Scholar
• 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 HDLc cholesterol. Atherosclerosis. 2004;177:113–18.
   PubMed Web of Science ®Google Scholar
• Popa C, Netea MG, Radstake T, Van der Meer JW, Stalenhoef AF, van Riel PL, et al. Influence of anti-tumour necrosis factor therapy on cardiovascular risk factors in patients with active rheumatoid arthritis. Ann Rheum Dis. 2005;64:303–5.
   PubMed Web of Science ®Google Scholar
• Vis M, Nurmohamed MT, Wolbink G, Voskuyl AE, de Koning M, van de Stadt R, et al. Short term effects of infliximab on the lipid profile in patients with rheumatoid arthritis. J Rheumatol. 2005;32:252–5.
   PubMed Web of Science ®Google Scholar
• Allanore Y, Kahan A, Sellam J, Ekindjian OG, Borderie D. Effects of repeated infliximab therapy on serum lipid profile in patients with refractory rheumatoid arthritis. Clin Chim Acta. 2006;365:143–8.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Juanatey C, Llorca J, Sanchez-Andrade A, Garcia-Porrua C, Martin J, Gonzalez-Gay MA. Short-term adalimumab therapy improves endothelial function in patients with rheumatoid arthritis refractory to infliximab. Clin Exp Rheumatol. 2006;24:309–12.
   PubMed Web of Science ®Google Scholar
• Dahlqvist SR, Engstrand S, Berglin E, Johnson O. Conversion towards an atherogenic lipid profile in rheumatoid arthritis patients during long-term infliximab therapy. Scand J Rheumatol. 2006;35:107–11.
   PubMed Web of Science ®Google Scholar
• Spanakis E, Sidiropoulos P, Papadakis J, Ganotakis E, Katsikas G, Karvounaris S, et al. Modest but sustained increase of serum high density lipoprotein cholesterol levels in patients with inflammatory arthritides treated with infliximab. J Rheumatol. 2006;33:2440–6.
   PubMed Web of Science ®Google Scholar
• Pérez-Galán MJ, Salvatierra-Ossorio J, Cáliz-Cáliz R, Guzmán-Ubeda MA. Influence of tumor necrosis alpha blockade with infliximab on lipid profile in patients with active rheumatoid arthritis. Med Clin (Barc). 2006;126:757.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Peters MJ, Vis M, van Halm VP, Wolbink GJ, Voskuyl AE, Lems WF, et al. Changes in lipid profile during infliximab and corticosteroid treatment in rheumatoid arthritis. Ann Rheum Dis. 2007;66:958–61.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Soubrier M, Jouanel P, Mathieu S, Poujol D, Claus D, Dubost JJ, et al. Effects of anti-tumor necrosis factor therapy on lipid profile in patients with rheumatoid arthritis. Joint Bone Spine. 2008;75:22–4.
   PubMed Web of Science ®Google Scholar
• Garcês SP, Parreira Santos MJ, Vinagre FM, Roque RM, da Silva JA. Anti-tumour necrosis factor agents and lipid profile: a class effect?. Ann Rheum Dis. 2008;67:895–6.
   PubMedGoogle Scholar
• Bosello S, Santoliquido A, Zoli A, Di Campli C, Flore R, Tondi P, et al. TNF-alpha blockade induces a reversible but transient effect on endothelial dysfunction in patients with long-standing severe rheumatoid arthritis. Clin Rheumatol. 2008;27:833–9.
   PubMed Web of Science ®Google Scholar
• Popa C, van Tits LJ, Barrera P, Lemmers HL, van den Hoogen FH, van Riel PL, et al. Anti-inflammatory therapy with tumour necrosis factor alpha inhibitors improves high-density lipoprotein cholesterol antioxidative capacity in rheumatoid arthritis patients. Ann Rheum Dis. 2009;68:868–72.
   PubMed Web of Science ®Google Scholar
• van Eijk IC, de Vries MK, Levels JH, Peters MJ, Huizer EE, Dijkmans BA, 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.
   PubMed Web of Science ®Google Scholar
• Wijbrandts CA, van Leuven SI, Boom HD, Gerlag DM, Stroes EG, Kastelein JJ, et al. Sustained changes in lipid profile and macrophage migration inhibitory factor levels after anti-tumour necrosis factor therapy in rheumatoid arthritis. Ann Rheum Dis. 2009;68:1316–21.
   PubMed Web of Science ®Google Scholar
• Mathieu S, Dubost JJ, Tournadre A, Malochet-Guinamand S, Ristori JM, Soubrier M. Effects of 14 weeks of TNF alpha blockade treatment on lipid profile in ankylosing spondylitis. Joint Bone Spine. 2010;77:50–2.
   PubMed Web of Science ®Google Scholar
• Syngle A, Vohra K, Sharma A, Kaur L. Endothelial dysfunction in ankylosing spondylitis improves after tumor necrosis factor-alpha blockade. Clin Rheumatol. 2010;29:763–70.
   PubMed Web of Science ®Google Scholar
• Jamnitski A, Visman IM, Peters MJ, Dijkmans BA, Voskuyl AE, Nurmohamed MT. Beneficial effect of 1-year etanercept treatment on the lipid profile in responding patients with rheumatoid arthritis: the ETRA study. Ann Rheum Dis. 2010;69:1929–33.
   PubMedGoogle Scholar
• Castro KR, Aikawa NE, Saad CG, Moraes JC, Medeiros AC, Mota LM, et al. Infliximab induces increase in triglyceride levels in psoriatic arthritis patients. Clin Dev Immunol. 2011;2011:352686.
   PubMedGoogle Scholar
• Taguchi H, Nishi K, Suzuki T, Okano Y. Anti-atherosclerotic effects of etanercept in rheumatoid arthritis patients. Nihon Rinsho Meneki Gakkai Kaishi. 2012;35:183–7.
   PubMedGoogle Scholar
• Mathieu S, Pereira B, Couderc M, Rabois E, Dubost JJ, Soubrier M. No significant changes in arterial stiffness in patients with ankylosing spondylitis after tumour necrosis factor alpha blockade treatment for 6 and 12 months. Rheumatology (Oxford). 2013;52:204–9.
   PubMed Web of Science ®Google Scholar
• Sandoo A, van Zanten JJ, Toms TE, Carroll D, Kitas GD. Anti-TNF-α therapy transiently improves high density lipoprotein cholesterol levels and microvascular endothelial function in patients with rheumatoid arthritis: a pilot study. BMC Musculoskelet Disord. 2012;13:127.
   PubMed Web of Science ®Google Scholar
• Di Minno MN, Peluso R, Iervolino S, Lupoli R, Russolillo A, Scarpa R, et al. Obesity and the prediction of minimal disease activity: a prospective study in psoriatic arthritis. Arthritis Care Res (Hoboken). 2013;65:141–7.
   PubMed Web of Science ®Google Scholar
• Iervolino S, Di Minno MN, Peluso R, Lofrano M, Russolillo A, Di Minno G, et al. Predictors of early minimal disease activity in patients with psoriatic arthritis treated with tumor necrosis factor-α blockers. J Rheumatol. 2012;39:568–73.
   PubMedGoogle Scholar
• Daïen CI, Duny Y, Barnetche T, Daurès JP, Combe B, Morel J. Effect of TNF inhibitors on lipid profile in rheumatoid arthritis: a systematic review with meta-analysis. Ann Rheum Dis. 2012;71:862–8.
   PubMed Web of Science ®Google Scholar
• Strang AC, Bisoendial RJ, Kootte RS, Schulte DM, Dallinga-Thie GM, Levels JH, et al. Pro-atherogenic lipid changes and decreased hepatic LDL receptor expression by tocilizumab in rheumatoid arthritis. Atherosclerosis. 2013;229:174–81.
   PubMed Web of Science ®Google Scholar
• Al-Shakarchi I, Gullick NJ, Scott DL. Current perspectives on tocilizumab for the treatment of rheumatoid arthritis: a review. Patient Prefer Adherence. 2013;7:653–66.
   PubMed Web of Science ®Google Scholar
• Raterman HG, Levels H, Voskuyl AE, Lems WF, Dijkmans BA, Nurmohamed MT. HDL protein composition alters from proatherogenic into less atherogenic and proinflammatory in rheumatoid arthritis patients responding to rituximab. Ann Rheum Dis. 2013; 72:560–5.
   PubMed Web of Science ®Google Scholar
• Kerekes G, Soltész P, Dér H, Veres K, Szabó Z, Végvári A, et al. Effects of rituximab treatment on endothelial dysfunction, carotid atherosclerosis, and lipid profile in rheumatoid arthritis. Clin Rheumatol. 2009;28:705–10.
   PubMed Web of Science ®Google Scholar
• Mathieu S, Pereira B, Dubost JJ, Lusson JR, Soubrier M. No significant change in arterial stiffness in RA after 6 months and 1 year of rituximab treatment. Rheumatology (Oxford). 2012;51:1107–11.
   PubMed Web of Science ®Google Scholar
• Third Report of the National Cholesterol Education Program (NCEP). Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation. 2002;106:3143–421.
   PubMed Web of Science ®Google Scholar
• Bass KM, Newschaffer CJ, Klag MJ, Bush TL. Plasma lipoprotein levels as predictors of cardiovascular death in women. Arch Intern Med. 1993;153:2209–16.
   PubMed Web of Science ®Google Scholar
• Russolillo A, Iervolino S, Peluso R, Lupoli R, Di Minno A, Pappone N, et al. Obesity and psoriatic arthritis: from pathogenesis to clinical outcome and management. Rheumatology (Oxford). 2013;52:62–7.
   PubMed Web of Science ®Google Scholar
• Lambert JE, Parks EJ. Postprandial metabolism of meal triglyceride in humans. Biochim Biophys Acta. 2012;1821:721–6.
   PubMed Web of Science ®Google Scholar
• Boers M, Nurmohamed MT, Doelman CJ, Lard LR, Verhoeven AC, Voskuyl AE, et al. Influence of glucocorticoids and disease activity on total and high density lipoprotein cholesterol in patients with rheumatoid arthritis. Ann Rheum Dis. 2003;62:842–5.
   PubMed Web of Science ®Google Scholar
• Georgiadis AN, Papavasiliou EC, Lourida ES, Alamanos Y, Kostara C, Tselepis AD, et al. Atherogenic lipid profile is a feature characteristic of patients with early rheumatoid arthritis: effect of early treatment–a prospective, controlled study. Arthritis Res Ther. 2006;8:R82.
   PubMed Web of Science ®Google Scholar
• Park YB, Choi HK, Kim MY, Lee WK, Song J, Kim DK, et al. Effects of antirheumatic therapy on serum lipid levels in patients with rheumatoid arthritis: a prospective study. Am J Med. 2002;113:188–93.
   PubMed Web of Science ®Google Scholar
• Hahn BH, Grossman J, Chen W, McMahon M. The pathogenesis of atherosclerosis in autoimmune rheumatic diseases: roles of inflammation and dyslipidemia. J Autoimmun. 2007;28:69–75.
   PubMed Web of Science ®Google Scholar
• Kiortsis DN, Mavridis AK, Filippatos TD, Vasakos S, Nikas SN, Drosos AA. Effects of infliximab treatment on lipoprotein profile in patients with rheumatoid arthritis and ankylosing spondylitis. J Rheumatol. 2006;33:921–3.
   PubMed Web of Science ®Google Scholar
• De Sanctis S, Marcovecchio ML, Gaspari S, Del Torto M, Mohn A, Chiarelli F, et al. Etanercept improves lipid profile and oxidative stress measures in patients with juvenile idiopathic arthritis. J Rheumatol. 2013;40:943–8.
   PubMedGoogle Scholar
• Daien CI, Fesler P, Du Cailar G, Daien V, Mura T, Dupuy AM, et al. Etanercept induces a decrease in left ventricular mass in patients with rheumatoid arthritis. Ann Rheum Dis. 2011;3:120.
   Google Scholar
• Di Minno MN, Iervolino S, Peluso R, Di Minno A, Ambrosino P, Scarpa R. Haemostatic and fibrinolytic changes are related to inflammatory conditions in patients with psoriatic arthritis. Effect of different treatments. J Rheumatol. [in press]
   Google Scholar
• Nordestgaard BG, Benn M, Schnohr P, Tybjaerg-Hansen A. Nonfasting triglycerides and risk of myocardial infarction, ischemic heart disease, and death in men and women. JAMA. 2007;298:299–308.
   PubMed Web of Science ®Google Scholar
• Freiberg JJ, Tybjaerg-Hansen A, Jensen JS, Nordestgaard BG. Nonfasting triglycerides and risk of ischemic stroke in the general population. JAMA. 2008;300:2142–52.
   PubMed Web of Science ®Google Scholar
• Schuitemaker GE, Dinant GJ, van der Pol GA, van Wersch JW. Relationship between smoking habits and low-density lipoprotein-cholesterol, high-density lipoprotein-cholesterol, and triglycerides in a hypercholesterolemic adult cohort, in relation to gender and age. Clin Exp Med. 2002;2:83–8.
   PubMedGoogle Scholar