Inflammation, lipid metabolism and cardiovascular risk in rheumatoid arthritis: A qualitative relationship?

World Journal of Orthopedics

Volumn 5, Issue 3, 2014, Pages 304-311

  García Gómez, Carmen ^a   Bianchi, Maria ^a   De la Fuente, Diana ^b   Badimon, Lina ^c   Padró, Teresa ^c   Corbella, Emili ^d   Pintó, Xavier ^d  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b HOSPITAL DE VILADECANS   (Spain)

^c BIOMEDICAL RESEARCH INSTITUTE SANT PAU IIB SANT PAU   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cardiovascular disease; Inflammation; Lipid metabolism; Lipoprotein(a); Lipoproteins; Oxidized low density lipoproteins; Proinflammatory high density lipoproteins; Rheumatoid arthritis

Indexed keywords

EID: 84906099391     PISSN: None     EISSN: 22185836     Source Type: Journal    
DOI: 10.5312/wjo.v5.i3.304     Document Type: Article

References (70)

1. Alamanos Y, Voulgari PV, Drosos AA. Incidence and prevalence of rheumatoid arthritis, based on the 1987 American College of Rheumatology criteria: a systematic review. Semin Arthritis Rheum 2006; 36: 182-188 [PMID: 17045630 DOI: 10.1016/j.semarthrit.2006.08.006]
2. Li R, Sun J, Ren LM, Wang HY, Liu WH, Zhang XW, Chen S, Mu R, He J, Zhao Y, Long L, Liu YY, Liu X, Lu XL, Li YH, Wang SY, Pan SS, Li C, Wang HY, Li ZG. Epidemiology of eight common rheumatic diseases in China: a large-scale cross-sectional survey in Beijing. Rheumatology (Oxford) 2012; 51: 721-729 [PMID: 22179737 DOI: 10.1093/rheumatology/ker370]
3. Ranganath VK, Maranian P, ElashoffDA, Woodworth T, Khanna D, Hahn T, Sarkisian C, Kremer JM, Furst DE, Paulus HE. Comorbidities are associated with poorer outcomes in community patients with rheumatoid arthritis. Rheumatology (Oxford) 2013; 52: 1809-1817 [PMID: 23813577 DOI: 10.1093/rheumatology/ket224]
4. Humphreys JH, Warner A, Chipping J, Marshall T, Lunt M, Symmons DP, Verstappen SM. Mortality trends in patients with early rheumatoid arthritis over 20 years: Results from the Norfolk Arthritis Register. Arthritis Care Res (Hoboken) 2014 Feb 4; Epub ahead of print [PMID: 24497371 DOI: 10.1002/acr.22296]
5. Symmons DP, Gabriel SE. Epidemiology of CVD in rheumatic disease, with a focus on RA and SLE. Nat Rev Rheumatol 2011; 7: 399-408 [PMID: 21629241 DOI: 10.1038/nrrheum.2011.75]
6. Kahlenberg JM, Kaplan MJ. Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu Rev Med 2013; 64: 249-263 [PMID: 23020882 DOI: 10.1146/annurev-med-060911-090007]
7. Avouac J, Meune C, Chenevier-Gobeaux C, Dieudé P, Borderie D, Lefevre G, Kahan A, Allanore Y. Inflammation and disease activity are associated with high circulating cardiac markers in rheumatoid arthritis independently of traditional cardiovascular risk factors. J Rheumatol 2014; 41: 248-255 [PMID: 24334650 DOI: 10.3899/jrheum.130713]
8. Koivuniemi R, Paimela L, Suomalainen R, Leirisalo-Repo M. Cardiovascular diseases in patients with rheumatoid arthritis. Scand J Rheumatol 2013; 42: 131-135 [PMID: 23244227 DOI: 10.3109/03009742.2012.723747]
9. Toms TE, Symmons DP, Kitas GD. Dyslipidaemia in rheumatoid arthritis: the role of inflammation, drugs, lifestyle and genetic factors. Curr Vasc Pharmacol 2010; 8: 301-326 [PMID: 19758115 DOI: 10.2174/157016110791112269]
10. Montecucco F, Mach F. Common inflammatory mediators orchestrate pathophysiological processes in rheumatoid arthritis and atherosclerosis. Rheumatology (Oxford) 2009; 48: 11-22 [PMID: 18927189 DOI: 10.1093/rheumatology/ken395]
11. 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: 460-469 [PMID: 19286905 DOI: 10.1136/ard.2008.101964]
12. Boekholdt SM, Arsenault BJ, Mora S, Pedersen TR, LaRosa JC, Nestel PJ, Simes RJ, Durrington P, Hitman GA, Welch KM, DeMicco DA, Zwinderman AH, Clearfield MB, Downs JR, Tonkin AM, Colhoun HM, Gotto AM, Ridker PM, Kastelein JJ. Association of LDL cholesterol, non-HDL cholesterol, and apolipoprotein B levels with risk of cardiovascular events among patients treated with statins: a metaanalysis. JAMA 2012; 307: 1302-1309 [PMID: 22453571 DOI: 10.1001/jama.2012.366]
13. Hahn BH, Grossman J, Chen W, McMahon M. The pathogenesis of atherosclerosis in autoimmune rheumatic diseases: 016/j.jaut.2007.02.004]
14. Choi HK, Seeger JD. Lipid profiles among US elderly with untreated rheumatoid arthritis--the Third National Health and Nutrition Examination Survey. J Rheumatol 2005; 32: 2311-2316 [PMID: 16331755]
15. Steiner G, Urowitz MB. Lipid profiles in patients with rheumatoid arthritis: mechanisms and the impact of treatment. Semin Arthritis Rheum 2009; 38: 372-381 [PMID: 18395771 DOI: 10.1016/j.semarthrit.2008.01.015]
16. García-Gómez C, Nolla JM, Valverde J, Narváez J, Corbella E, Pintó X. High HDL-cholesterol in women with rheumatoid arthritis on low-dose glucocorticoid therapy. Eur J Clin Invest 2008; 38: 686-692 [PMID: 18837746 DOI: 10.1111/j.1365-2362.2008.01994.x]
17. Williams PT, Feldman DE. Prospective study of coronary heart disease vs. HDL2, HDL3, and other lipoproteins in Gofman's Livermore Cohort. Atherosclerosis 2011; 214: 196-202 [PMID: 21109246 DOI: 10.1016/j.atherosclerosis.201 0.10.024]
18. Yang CY, Raya JL, Chen HH, Chen CH, Abe Y, Pownall HJ, Taylor AA, Smith CV. Isolation, characterization, and functional assessment of oxidatively modified subfractions of circulating low-density lipoproteins. Arterioscler Thromb Vasc Biol 2003; 23: 1083-1090 [PMID: 12689919]
19. Toms TE, Panoulas VF, Kitas GD. Dyslipidaemia in rheumatological autoimmune diseases. Open Cardiovasc Med J 2011; 5: 64-75 [PMID: 21660202 DOI: 10.2174/1874192401105 010064]
20. Rizzo M, Spinas GA, Cesur M, Ozbalkan Z, Rini GB, Berneis K. Atherogenic lipoprotein phenotype and LDL size and subclasses in drug-naïve patients with early rheumatoid arthritis. Atherosclerosis 2009; 207: 502-506 [PMID: 19643412 DOI: 10.1016/j.atherosclerosis.2009.07.015]
21. García-Gómez C, Nolla JM, Valverde J, Gómez-Gerique JA, Castro MJ, Pintó X. Conventional lipid profile and lipoprotein(a) concentrations in treated patients with rheumatoid arthritis. J Rheumatol 2009; 36: 1365-1370 [PMID: 19369465 DOI: 10.3899/jrheum.080928]
22. Zhang C, Li X, Niu D, Zi R, Wang C, Han A, Wang X, Li K, Wang J. Increased serum levels of ß2-GPI-Lp(a) complexes and their association with premature atherosclerosis in patients with rheumatoid arthritis. Clin Chim Acta 2011; 412: 1332-1336 [PMID: 21473861 DOI: 10.1016/j.cca.2011.03.029]
23. Movva R, Rader DJ. Laboratory assessment of HDL heterogeneity and function. Clin Chem 2008; 54: 788-800 [PMID: 18375481 DOI: 10.1373/clinchem.2007.101923]
24. Superko HR, Pendyala L, Williams PT, Momary KM, King SB, Garrett BC. High-density lipoprotein subclasses and their relationship to cardiovascular disease. J Clin Lipidol 2012; 6: 496-523 [PMID: 23312047 DOI: 10.1016/j.jacl.2012.03.001]
25. Rader DJ. Molecular regulation of HDL metabolism and function: implications for novel therapies. J Clin Invest 2006; 116: 3090-3100 [PMID: 17143322]
26. Rosenson RS, Brewer HB, Davidson WS, Fayad ZA, Fuster V, Goldstein J, Hellerstein M, Jiang XC, Phillips MC, Rader DJ, Remaley AT, Rothblat GH, Tall AR, Yvan-Charvet L. Cholesterol efflux and atheroprotection: advancing the concept of reverse cholesterol transport. Circulation 2012; 125: 1905-1919 [PMID: 22508840 DOI: 10.1161/CIRCULATIONAHA. 111.066589]
27. Breton CV, Yin F, Wang X, Avol E, Gilliland FD, Araujo JA. HDL anti-oxidant function associates with LDL level in young adults. Atherosclerosis 2014; 232: 165-170 [PMID: 24401232 DOI: 10.1016/j.atherosclerosis.2013.10.034]
28. Huang Y, Wu Z, Riwanto M, Gao S, Levison BS, Gu X, Fu X, Wagner MA, Besler C, Gerstenecker G, Zhang R, Li XM, DiDonato AJ, Gogonea V, Tang WH, Smith JD, Plow EF, Fox PL, Shih DM, Lusis AJ, Fisher EA, DiDonato JA, Landmesser U, Hazen SL. Myeloperoxidase, paraoxonase-1, and HDL form a functional ternary complex. J Clin Invest 2013; 123: 3815-3828 [PMID: 23908111 DOI: 10.1172/JCI67478]
29. Barter PJ, Caulfield M, Eriksson M, Grundy SM, Kastelein JJ, Komajda M, Lopez-Sendon J, Mosca L, Tardif JC, Waters DD, Shear CL, Revkin JH, Buhr KA, Fisher MR, Tall AR, Brewer B. Effects of torcetrapib in patients at high risk for coronary events. N Engl J Med 2007; 357: 2109-2122 [PMID: 17984165 DOI: 10.1056/NEJMoa0706628]
30. Ansell BJ, Fonarow GC, Navab M, Fogelman AM. Modifying the anti-inflammatory effects of high-density lipoprotein. Curr Atheroscler Rep 2007; 9: 57-63 [PMID: 17169248]
31. G HB, Rao VS, Kakkar VV. Friend Turns Foe: Transformation of Anti-Inflammatory HDL to Proinflammatory HDL during Acute-Phase Response. Cholesterol 2011; 2011: 274629 [PMID: 21490770 DOI: 10.1155/2011/274629]
32. Hahn BH, Grossman J, Ansell BJ, Skaggs BJ, McMahon M. Altered lipoprotein metabolism in chronic inflammatory states: proinflammatory high-density lipoprotein and accelerated atherosclerosis in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Res Ther 2008; 10: 213 [PMID: 18828865 DOI: 10.1186/ar2471]
33. Ferraz-Amaro I, González-Gay MA, García-Dopico JA, Díaz-González F. Cholesteryl ester transfer protein in patients with rheumatoid arthritis. J Rheumatol 2013; 40: 1040-1047 [PMID: 23678159 DOI: 10.3899/jrheum.121507]
34. McMahon M, Grossman J, FitzGerald J, Dahlin-Lee E, Wallace DJ, Thong BY, Badsha H, Kalunian K, Charles C, Navab M, Fogelman AM, Hahn BH. Proinflammatory high-density lipoprotein as a biomarker for atherosclerosis in patients with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 2006; 54: 2541-2549 [PMID: 16868975 DOI: 10.1002/art.21976]
35. 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 [PMID: 22991486]
36. Popa C, van Tits LJ, Barrera P, Lemmers HL, Den Hoogen VFH, van Riel PL, Radstake TR, Netea MG, Roest M, Stalenhoef AF. 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: 868-872 [PMID: 18635596 DOI: 10.1136/ard.2008.092171]
37. Jamnitski A, Levels JH, Den Oever VIA, Nurmohamed MT. High-density lipoprotein profiling changes in patients with rheumatoid arthritis treated with tumor necrosis factor inhibitors: a cohort study. J Rheumatol 2013; 40: 825-830 [PMID: 23637327 DOI: 10.3899/jrheum.121358]
38. 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: 560-565 [PMID: 22589377 DOI: 10.1136/annrheumdis-2011-201228]
39. Yamashita S, Tsubakio-Yamamoto K, Ohama T, Nakagawa- Toyama Y, Nishida M. Molecular mechanisms of HDL-cholesterol elevation by statins and its effects on HDL functions. J Atheroscler Thromb 2010; 17: 436-451 [PMID: 20513953]
40. Charles-Schoeman C, Khanna D, Furst DE, McMahon M, Reddy ST, Fogelman AM, Paulus HE, Park GS, Gong T, Ansell BJ. Effects of high-dose atorvastatin on antiinflammatory properties of high density lipoprotein in patients with rheumatoid arthritis: a pilot study. J Rheumatol 2007; 34: 1459-1464 [PMID: 17552046]
41. Nikolic D, Katsiki N, Montalto G, Isenovic ER, Mikhailidis DP, Rizzo M. Lipoprotein subfractions in metabolic syndrome and obesity: clinical significance and therapeutic approaches. Nutrients 2013; 5: 928-948 [PMID: 23507795 DOI: 10.3390/nu5030928.]
42. Björkbacka H, Fredrikson GN, Nilsson J. Emerging biomarkers and intervention targets for immune-modulation of atherosclerosis-a review of the experimental evidence. Atherosclerosis 2013; 227: 9-17 [PMID: 23177975 DOI: 10.1016/j.atherosclerosis.2012.10.074]
43. Delporte C, Van Antwerpen P, Vanhamme L, Roumeguère T, Zouaoui Boudjeltia K. Low-density lipoprotein modified by myeloperoxidase in inflammatory pathways and clinical studies. Mediators Inflamm 2013; 2013: 971579 [PMID: 23983406 DOI: 10.1155/2013/971579]
44. Mayr M, Kiechl S, Tsimikas S, Miller E, Sheldon J, Willeit J, Witztum JL, Xu Q. Oxidized low-density lipoprotein autoantibodies, chronic infections, and carotid atherosclerosis in a population-based study. J Am Coll Cardiol 2006; 47: 2436-2443 [PMID: 16781371]
45. Peters MJ, van Halm VP, Nurmohamed MT, Damoiseaux J, Tervaert JW, Twisk JW, Dijkmans BA, Voskuyl AE. Relations between autoantibodies against oxidized low-density lipoprotein, inflammation, subclinical atherosclerosis, and cardiovascular disease in rheumatoid arthritis. J Rheumatol 2008; 35: 1495-1499 [PMID: 18597411]
46. Fuhrman B. Regulation of hepatic paraoxonase-1 expression. J Lipids 2012; 2012: 684010 [PMID: 22548179 DOI: 10.1155/2012/684010]
47. Makedou KG, Mikhailidis DP, Makedou A, Iliadis S, Kourtis A, Vavatsi-Christaki N, Papageorgiou GE. Lipid profile, low-density lipoprotein oxidation and ceruloplasmin in the progeny of families with a positive history of cardiovascular diseases and/or hyperlipidemia. Angiology 2009; 60: 455-461 [PMID: 19648144 DOI: 10.1177/0003319709338174]
48. Balagopalakrishna C, Paka L, Pillarisetti S, Goldberg IJ. Lipolysis-induced iron release from diferric transferrin: Pos- sible role of lipoprotein lipase in LDL oxidation. J Lipid Res 1999; 40: 1347-1356 [PMID: 10393220]
49. Winyard PG, Tatzber F, Esterbauer H, Kus ML, Blake DR, Morris CJ. Presence of foam cells containing oxidised low density lipoprotein in the synovial membrane from patients with rheumatoid arthritis. Ann Rheum Dis 1993; 52: 677-680 [PMID: 8239763 DOI: 10.1136/ard.52.9.677]
50. Dai L, Lamb DJ, Leake DS, Kus ML, Jones HW, Morris CJ, Winyard PG. Evidence for oxidised low density lipoprotein in synovial fluid from rheumatoid arthritis patients. Free Radic Res 2000; 32: 479-486 [PMID: 10798713 DOI: 10.1080/1 0715760000300481]
51. Kim SH, Lee CK, Lee EY, Park SY, Cho YS, Yoo B, Moon HB. Serum oxidized low-density lipoproteins in rheumatoid arthritis. Rheumatol Int 2004; 24: 230-233 [PMID: 14628150 DOI: 10.1007/s00296-003-0358-4]
52. Vuilleumier N, Bratt J, Alizadeh R, Jogestrand T, Hafström I, Frostegård J. Anti-apoA-1 IgG and oxidized LDL are raised in rheumatoid arthritis (RA): potential associations with cardiovascular disease and RA disease activity. Scand J Rheumatol 2010; 39: 447-453 [PMID: 20604674 DOI: 10.3109/03009741003742755]
53. Ajeganova S, de Faire U, Jogestrand T, Frostegård J, Hafström I. Carotid atherosclerosis, disease measures, oxidized low-density lipoproteins, and atheroprotective natural antibodies for cardiovascular disease in early rheumatoid arthritis -- an inception cohort study. J Rheumatol 2012; 39: 1146-1154 [PMID: 22589258 DOI: 10.3899/jrheum.111334]
54. Profumo E, Di Franco M, Buttari B, Masella R, Filesi C, Tosti ME, Scrivo R, Scarno A, Spadaro A, Saso L, Riganò R. Biomarkers of subclinical atherosclerosis in patients with autoimmune disorders. Mediators Inflamm 2012; 2012: 503942 [PMID: 22529523 DOI: 10.1155/2012/503942]
55. Ahmed HM, Youssef M, Mosaad YM. Antibodies against oxidized low-density lipoprotein are associated with subclinical atherosclerosis in recent-onset rheumatoid arthritis. Clin Rheumatol 2010; 29: 1237-1243 [PMID: 20354747 DOI: 10.1007/s10067-010-1436-0]
56. Ajeganova S, Fiskesund R, de Faire U, Hafström I, Frostegård J. Effect of biological therapy on levels of atheroprotective antibodies against phosphorylcholine and apolipoproteins in rheumatoid arthritis-a one year study. Clin Exp Rheumatol 2011; 29: 942-950 [PMID: 22153361]
57. Berg K. A new serum type system in man--the lp system. Acta Pathol Microbiol Scand 1963; 59: 369-382 [PMID: 14064818 DOI: 10.1111/j.1699-0463.1963.tb01808.x]
58. Enkhmaa B, Anuurad E, Zhang W, Tran T, Berglund L. Lipoprotein(a): genotype-phenotype relationship and impact on atherogenic risk. Metab Syndr Relat Disord 2011; 9: 411-418 [PMID: 21749171 DOI: 10.1089/met.2011.0026]
59. Lanktree MB, Rajakumar C, Brunt JH, Koschinsky ML, Connelly PW, Hegele RA. Determination of lipoprotein(a) kringle repeat number from genomic DNA: copy number variation genotyping using qPCR. J Lipid Res 2009; 50: 768-772 [PMID: 19060253 DOI: 10.1194/jlr. D800050-JLR200]
60. Dumitrescu L, Glenn K, Brown-Gentry K, Shephard C, Wong M, Rieder MJ, Smith JD, Nickerson DA, Crawford DC. Variation in LPA is associated with Lp(a) levels in three populations from the Third National Health and Nutrition Examination Survey. PLoS One 2011; 6: e16604 [PMID: 21305047 DOI: 10.1371/journal.pone.0016604]
61. Clarke R, Peden JF, Hopewell JC, Kyriakou T, Goel A, Heath SC, Parish S, Barlera S, Franzosi MG, Rust S, Bennett D, Silveira A, Malarstig A, Green FR, Lathrop M, Gigante B, Leander K, de Faire U, Seedorf U, Hamsten A, Collins R, Watkins H, Farrall M. Genetic variants associated with Lp(a) lipoprotein level and coronary disease. N Engl J Med 2009; 361: 2518-2528 [PMID: 20032323 DOI: 10.1056/NEJMoa0902604]
62. Scanu AM, Bamba R. Niacin and lipoprotein(a): facts, uncertainties, and clinical considerations. Am J Cardiol 2008; 101: 44B-47B [PMID: 18375241 DOI: 10.1016/j.amjcard.2008.02.031]
63. Kurian AK, Cardarelli KM. Racial and ethnic differences in cardiovascular disease risk factors: a systematic review. Ethn Dis 2007; 17: 143-152 [PMID: 17274224]
64. Kronenberg F, Utermann G. Lipoprotein(a): resurrected by genetics. J Intern Med 2013; 273: 6-30 [PMID: 22998429 DOI: 10.1111/j.1365-2796.2012.02592.x]
65. Emerging Risk Factors Collaboration, Erqou S, Kaptoge S, Perry PL, Di Angelantonio E, Thompson A, White IR, Marcovina SM, Collins R, Thompson SG, Danesh J. Lipoprotein(a) concentration and the risk of coronary heart disease, stroke, and nonvascular mortality. JAMA 2009; 302: 412-423 [PMID: 19622820 DOI: 10.1001/jama.2009.1063]
66. Liu L, Boffa MB, Koschinsky ML. Apolipoprotein(a) inhibits in vitro tube formation in endothelial cells: identification of roles for Kringle V and the plasminogen activation system. PLoS One 2013; 8: e52287 [PMID: 23326327 DOI: 10.1371/journal.pone.0052287]
67. Koschinsky ML. Lipoprotein(a) and atherosclerosis: new perspectives on the mechanism of action of an enigmatic lipoprotein. Curr Atheroscler Rep 2005; 7: 389-395 [PMID: 16105483 DOI: 10.1007/s11883-005-0052-y]
68. Missala I, Kassner U, Steinhagen-Thiessen E. A Systematic Literature Review of the Association of Lipoprotein(a) and Autoimmune Diseases and Atherosclerosis. Int J Rheumatol 2012; 2012: 480784 [PMID: 23304154 DOI: 10.1155/2012/480784]
69. Hjeltnes G, Hollan I, Førre O, Wiik A, Lyberg T, Mikkelsen K, Agewall S. Serum levels of lipoprotein(a) and E-selectin are reduced in rheumatoid arthritis patients treated with methotrexate or methotrexate in combination with TNF-a-inhibitor. Clin Exp Rheumatol 2013; 31: 415-421 [PMID: 23465067]
70. Schultz O, Oberhauser F, Saech J, Rubbert-Roth A, Hahn M, Krone W, Laudes M. Effects of inhibition of interleukin- 6 signalling on insulin sensitivity and lipoprotein (a) levels in human subjects with rheumatoid diseases. PLoS One 2010; 5: e14328 [PMID: 21179199 DOI: 10.1371/journal. pone.0014328]