Skip to main content

Advertisement

Log in

Cutaneous lupus erythematosus and cardiovascular disease: current knowledge and insights into pathogenesis

  • Review Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Multiple autoinflammatory diseases, including psoriasis, psoriatic arthritis, and systemic lupus erythematosus, have been linked to increased risk of cardiovascular disease. Inflammation is known to play a key role in the pathogenesis of atherosclerosis, thus the contribution of systemic immune dysregulation, which characterizes such inflammatory conditions, towards the development of cardiovascular disease has garnered considerable interest. Cutaneous lupus erythematosus (CLE) is a chronic inflammatory skin disease, but risk of cardiovascular disease amongst patients with cutaneous lupus is less well known. Observational studies, including those of large nationwide cohorts, have been conducted to examine cardiovascular disease risk in CLE, with varying findings. As with other inflammatory diseases, immunologic mechanisms may provide plausible causal links between CLE and cardiovascular risk. On a macrolevel, several disease-related characteristics may also contribute to cardiovascular risk amongst CLE patients. This represents an area of research that should be prioritized, as understanding cardiovascular disease risk has important clinical implications for CLE patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data availability

Not applicable.

References

  1. Tebbe B, Orfanos CE (1997) Epidemiology and socioeconomic impact of skin disease in lupus erythematosus. Lupus 6(2):96–104. https://doi.org/10.1177/096120339700600204

    Article  CAS  PubMed  Google Scholar 

  2. Gilliam JN, Sontheimer RD (1981) Distinctive cutaneous subsets in the spectrum of lupus erythematosus. J Am Acad Dermatol 4(4):471–475. https://doi.org/10.1016/s0190-9622(81)80261-7

    Article  CAS  PubMed  Google Scholar 

  3. Okon LG, Werth VP (2013) Cutaneous lupus erythematosus: diagnosis and treatment. Best Pract Res Clin Rheumatol 27(3):391–404. https://doi.org/10.1016/j.berh.2013.07.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Werth VP (2007) Cutaneous lupus: insights into pathogenesis and disease classification. Bull NYU Hosp Jt Dis 65(3):200–204

    PubMed  Google Scholar 

  5. Stannard JN, Kahlenberg JM (2016) Cutaneous lupus erythematosus: updates on pathogenesis and associations with systemic lupus. Curr Opin Rheumatol 28(5):453–459. https://doi.org/10.1097/BOR.0000000000000308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wenzel J, Tüting T (2007) Identification of type I interferon-associated inflammation in the pathogenesis of cutaneous lupus erythematosus opens up options for novel therapeutic approaches. Exp Dermatol 16(5):454–463. https://doi.org/10.1111/j.1600-0625.2007.00556.x

    Article  CAS  PubMed  Google Scholar 

  7. Popovic K, Ek M, Espinosa A, Padyukov L, Harris HE, Wahren-Herlenius M, Nyberg F (2005) Increased expression of the novel proinflammatory cytokine high mobility group box chromosomal protein 1 in skin lesions of patients with lupus erythematosus. Arthritis Rheum 52(11):3639–3645. https://doi.org/10.1002/art.21398

    Article  CAS  PubMed  Google Scholar 

  8. Franz B, Fritzsching B, Riehl A, Oberle N, Klemke CD, Sykora J, Quick S, Stumpf C, Hartmann M, Enk A, Ruzicka T, Krammer PH, Suri-Payer E, Kuhn A (2007) Low number of regulatory T cells in skin lesions of patients with cutaneous lupus erythematosus. Arthritis Rheum 56(6):1910–1920. https://doi.org/10.1002/art.22699

    Article  CAS  PubMed  Google Scholar 

  9. Aviña-Zubieta JA, To F, Vostretsova K, De Vera M, Sayre EC, Esdaile JM (2017) Risk of myocardial infarction and stroke in newly diagnosed systemic lupus Erythematosus: a general population-based study. Arthritis Care Res (Hoboken) 69(6):849–856. https://doi.org/10.1002/acr.23018

    Article  Google Scholar 

  10. Hak AE, Karlson EW, Feskanich D, Stampfer MJ, Costenbader KH (2009) Systemic lupus erythematosus and the risk of cardiovascular disease: results from the nurses' health study. Arthritis Rheum 61(10):1396–1402. https://doi.org/10.1002/art.24537

    Article  PubMed  PubMed Central  Google Scholar 

  11. Armstrong EJ, Harskamp CT, Armstrong AW (2013) Psoriasis and major adverse cardiovascular events: a systematic review and meta-analysis of observational studies. J Am Heart Assoc 2(2):e000062. https://doi.org/10.1161/JAHA.113.000062

    Article  PubMed  PubMed Central  Google Scholar 

  12. Ogdie A, Yu Y, Haynes K, Love TJ, Maliha S, Jiang Y, Troxel AB, Hennessy S, Kimmel SE, Margolis DJ, Choi H, Mehta NN, Gelfand JM (2015) Risk of major cardiovascular events in patients with psoriatic arthritis, psoriasis and rheumatoid arthritis: a population-based cohort study. Ann Rheum Dis 74(2):326–332. https://doi.org/10.1136/annrheumdis-2014-205675

    Article  PubMed  Google Scholar 

  13. Avina-Zubieta JA, Thomas J, Sadatsafavi M, Lehman AJ, Lacaille D (2012) Risk of incident cardiovascular events in patients with rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis 71(9):1524–1529. https://doi.org/10.1136/annrheumdis-2011-200726

    Article  PubMed  Google Scholar 

  14. Han C, Robinson DW, 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(11):2167–2172

    PubMed  Google Scholar 

  15. Hansson GK (2005) Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352(16):1685–1695. https://doi.org/10.1056/NEJMra043430

    Article  CAS  PubMed  Google Scholar 

  16. Willerson JT, Ridker PM (2004) Inflammation as a cardiovascular risk factor. Circulation 109(21 Suppl 1):II2–I10. https://doi.org/10.1161/01.CIR.0000129535.04194.38

    Article  PubMed  Google Scholar 

  17. van Leuven SI, Franssen R, Kastelein JJ, Levi M, Stroes ES, Tak PP (2008) Systemic inflammation as a risk factor for atherothrombosis. Rheumatology (Oxford) 47(1):3–7. https://doi.org/10.1093/rheumatology/kem202

    Article  CAS  Google Scholar 

  18. Hesselvig JH, Ahlehoff O, Dreyer L, Gislason G, Kofoed K (2017) Cutaneous lupus erythematosus and systemic lupus erythematosus are associated with clinically significant cardiovascular risk: a Danish nationwide cohort study. Lupus 26(1):48–53. https://doi.org/10.1177/0961203316651739

    Article  PubMed  Google Scholar 

  19. Singh AG, Crowson CS, Singh S, Denis M, Davis P, Maradit-Kremers H, Matteson EL, Chowdhary VR (2016) Risk of cerebrovascular accidents and ischemic heart disease in cutaneous lupus Erythematosus: a population-based cohort study. Arthritis Care Res (Hoboken) 68(11):1664–1670. https://doi.org/10.1002/acr.22892

    Article  Google Scholar 

  20. Zöller B, Li X, Sundquist J, Sundquist K (2012) Risk of subsequent coronary heart disease in patients hospitalized for immune-mediated diseases: a nationwide follow-up study from Sweden. PLoS One 7(3):e33442. https://doi.org/10.1371/journal.pone.0033442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zöller B, Li X, Sundquist J, Sundquist K (2012) Risk of subsequent ischemic and hemorrhagic stroke in patients hospitalized for immune-mediated diseases: a nationwide follow-up study from Sweden. BMC Neurol 12:41. https://doi.org/10.1186/1471-2377-12-41

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ahlehoff O, Wu JJ, Raunsø J, Kristensen SL, Khalid U, Kofoed K, Gislason G (2017) Cutaneous lupus erythematosus and the risk of deep venous thrombosis and pulmonary embolism: a Danish nationwide cohort study. Lupus 26(13):1435–1439. https://doi.org/10.1177/0961203317716306

    Article  CAS  PubMed  Google Scholar 

  23. Murthy SK, Nguyen GC (2011) Venous thromboembolism in inflammatory bowel disease: an epidemiological review. Am J Gastroenterol 106(4):713–718. https://doi.org/10.1038/ajg.2011.53

    Article  PubMed  Google Scholar 

  24. Grainge MJ, West J, Card TR (2010) Venous thromboembolism during active disease and remission in inflammatory bowel disease: a cohort study. Lancet 375(9715):657–663. https://doi.org/10.1016/S0140-6736(09)61963-2

    Article  PubMed  Google Scholar 

  25. Libby P (2002) Inflammation in atherosclerosis. Nature 420(6917):868–874. https://doi.org/10.1038/nature01323

    Article  CAS  PubMed  Google Scholar 

  26. Hansson GK, Libby P (2006) The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 6(7):508–519. https://doi.org/10.1038/nri1882

    Article  CAS  PubMed  Google Scholar 

  27. Skålén K, Gustafsson M, Rydberg EK, Hultén LM, Wiklund O, Innerarity TL, Borén J (2002) Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 417(6890):750–754. https://doi.org/10.1038/nature00804

    Article  CAS  PubMed  Google Scholar 

  28. Leitinger N (2003) Oxidized phospholipids as modulators of inflammation in atherosclerosis. Curr Opin Lipidol 14(5):421–430. https://doi.org/10.1097/00041433-200310000-00002

    Article  CAS  PubMed  Google Scholar 

  29. Frostegård J, Ulfgren AK, Nyberg P, Hedin U, Swedenborg J, Andersson U, Hansson GK (1999) Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 145(1):33–43. https://doi.org/10.1016/s0021-9150(99)00011-8

    Article  PubMed  Google Scholar 

  30. Uyemura K, Demer LL, Castle SC, Jullien D, Berliner JA, Gately MK, Warrier RR, Pham N, Fogelman AM, Modlin RL (1996) Cross-regulatory roles of interleukin (IL)-12 and IL-10 in atherosclerosis. J Clin Invest 97(9):2130–2138. https://doi.org/10.1172/JCI118650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hansson GK (2001) Immune mechanisms in atherosclerosis. Arterioscler Thromb Vasc Biol 21(12):1876–1890. https://doi.org/10.1161/hq1201.100220

    Article  CAS  PubMed  Google Scholar 

  32. Szabo SJ, Sullivan BM, Peng SL, Glimcher LH (2003) Molecular mechanisms regulating Th1 immune responses. Annu Rev Immunol 21:713–758. https://doi.org/10.1146/annurev.immunol.21.120601.140942

    Article  CAS  PubMed  Google Scholar 

  33. Trieu N, Eslick GD (2014) Alopecia and its association with coronary heart disease and cardiovascular risk factors: a meta-analysis. Int J Cardiol 176(3):687–695. https://doi.org/10.1016/j.ijcard.2014.07.079

    Article  PubMed  Google Scholar 

  34. Silverberg JI (2015) Association between adult atopic dermatitis, cardiovascular disease, and increased heart attacks in three population-based studies. Allergy 70(10):1300–1308. https://doi.org/10.1111/all.12685

    Article  CAS  PubMed  Google Scholar 

  35. Jabbari A, Suárez-Fariñas M, Fuentes-Duculan J, Gonzalez J, Cueto I, Franks AG, Krueger JG (2014) Dominant Th1 and minimal Th17 skewing in discoid lupus revealed by transcriptomic comparison with psoriasis. J Invest Dermatol 134(1):87–95. https://doi.org/10.1038/jid.2013.269

    Article  CAS  PubMed  Google Scholar 

  36. Klimpel GR, Infante AJ, Patterson J, Hess CB, Asuncion M (1990) Virus-induced interferon alpha/beta (IFN-alpha/beta) production by T cells and by Th1 and Th2 helper T cell clones: a study of the immunoregulatory actions of IFN-gamma versus IFN-alpha/beta on functions of different T cell populations. Cell Immunol 128(2):603–618. https://doi.org/10.1016/0008-8749(90)90052-s

    Article  CAS  PubMed  Google Scholar 

  37. Wenzel J, Wörenkämper E, Freutel S, Henze S, Haller O, Bieber T, Tüting T (2005) Enhanced type I interferon signalling promotes Th1-biased inflammation in cutaneous lupus erythematosus. J Pathol 205(4):435–442. https://doi.org/10.1002/path.1721

    Article  CAS  PubMed  Google Scholar 

  38. Dey-Rao R, Sinha AA (2015) Genome-wide transcriptional profiling of chronic cutaneous lupus erythematosus (CCLE) peripheral blood identifies systemic alterations relevant to the skin manifestation. Genomics 105(2):90–100. https://doi.org/10.1016/j.ygeno.2014.11.004

    Article  CAS  PubMed  Google Scholar 

  39. Foering K, Chang AY, Piette EW, Cucchiara A, Okawa J, Werth VP (2013) Characterization of clinical photosensitivity in cutaneous lupus erythematosus. J Am Acad Dermatol 69(2):205–213. https://doi.org/10.1016/j.jaad.2013.03.015

    Article  PubMed  PubMed Central  Google Scholar 

  40. Bashir MM, Sharma MR, Werth VP (2009) UVB and proinflammatory cytokines synergistically activate TNF-alpha production in keratinocytes through enhanced gene transcription. J Invest Dermatol 129(4):994–1001. https://doi.org/10.1038/jid.2008.332

    Article  CAS  PubMed  Google Scholar 

  41. Zampieri S, Alaibac M, Iaccarino L, Rondinone R, Ghirardello A, Sarzi-Puttini P, Peserico A, Doria A (2006) Tumour necrosis factor alpha is expressed in refractory skin lesions from patients with subacute cutaneous lupus erythematosus. Ann Rheum Dis 65(4):545–548. https://doi.org/10.1136/ard.2005.039362

    Article  CAS  PubMed  Google Scholar 

  42. Kleinbongard P, Heusch G, Schulz R (2010) TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther 127(3):295–314. https://doi.org/10.1016/j.pharmthera.2010.05.002

    Article  CAS  PubMed  Google Scholar 

  43. von Stebut E, Boehncke WH, Ghoreschi K, Gori T, Kaya Z, Thaci D, Schäffler A (2019) IL-17A in psoriasis and beyond: cardiovascular and metabolic implications. Front Immunol 10:3096. https://doi.org/10.3389/fimmu.2019.03096

    Article  CAS  Google Scholar 

  44. Golden JB, McCormick TS, Ward NL (2013) IL-17 in psoriasis: implications for therapy and cardiovascular co-morbidities. Cytokine 62(2):195–201. https://doi.org/10.1016/j.cyto.2013.03.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Tanasescu C, Balanescu E, Balanescu P, Olteanu R, Badea C, Grancea C, Vagu C, Bleotu C, Ardeleanu C, Georgescu A (2010) IL-17 in cutaneous lupus erythematosus. Eur J Intern Med 21(3):202–207. https://doi.org/10.1016/j.ejim.2010.03.004

    Article  CAS  PubMed  Google Scholar 

  46. Grönhagen CM, Fored CM, Granath F, Nyberg F (2011) Cutaneous lupus erythematosus and the association with systemic lupus erythematosus: a population-based cohort of 1088 patients in Sweden. Br J Dermatol 164(6):1335–1341. https://doi.org/10.1111/j.1365-2133.2011.10272.x

    Article  PubMed  Google Scholar 

  47. Callen JP (1985) Systemic lupus erythematosus in patients with chronic cutaneous (discoid) lupus erythematosus. Clinical and laboratory findings in seventeen patients. J Am Acad Dermatol 12(2 Pt 1):278–288. https://doi.org/10.1016/s0190-9622(85)80036-0

    Article  CAS  PubMed  Google Scholar 

  48. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA, Jansen-McWilliams L, D'Agostino RB, Kuller LH (1997) Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham study. Am J Epidemiol 145(5):408–415. https://doi.org/10.1093/oxfordjournals.aje.a009122

    Article  CAS  PubMed  Google Scholar 

  49. Björnådal L, Yin L, Granath F, Klareskog L, Ekbom A (2004) Cardiovascular disease a hazard despite improved prognosis in patients with systemic lupus erythematosus: results from a Swedish population based study 1964-95. J Rheumatol 31(4):713–719

    PubMed  Google Scholar 

  50. Sattar N, Gaw A, Scherbakova O, Ford I, O'Reilly DS, Haffner SM, Isles C, Macfarlane PW, Packard CJ, Cobbe SM, Shepherd J (2003) Metabolic syndrome with and without C-reactive protein as a predictor of coronary heart disease and diabetes in the West of Scotland coronary prevention study. Circulation 108(4):414–419. https://doi.org/10.1161/01.CIR.0000080897.52664.94

    Article  CAS  PubMed  Google Scholar 

  51. Alexander CM, Landsman PB, Teutsch SM, Haffner SM, III) TNHaNESN, (NCEP) NCEP (2003) NCEP-defined metabolic syndrome, diabetes, and prevalence of coronary heart disease among NHANES III participants age 50 years and older. Diabetes 52 (5):1210–1214. doi:https://doi.org/10.2337/diabetes.52.5.1210

  52. Malik S, Wong ND, Franklin SS, Kamath TV, L'Italien GJ, Pio JR, Williams GR (2004) Impact of the metabolic syndrome on mortality from coronary heart disease, cardiovascular disease, and all causes in United States adults. Circulation 110(10):1245–1250. https://doi.org/10.1161/01.CIR.0000140677.20606.0E

    Article  PubMed  Google Scholar 

  53. Akarsu S, Ozbagcivan O, Semiz F, Aktan S (2017) High prevalence of metabolic syndrome in patients with discoid lupus Erythematosus: a cross-sectional, case-control study. J Immunol Res 2017:3972706–3972708. https://doi.org/10.1155/2017/3972706

    Article  PubMed  PubMed Central  Google Scholar 

  54. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC, Prevention IDFTFoEa, Hational Heart Ln, and Blood Institute, Association AH, Federation WH, Society IA, Obesity IAftSo (2009) Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; National Heart, Lung, and Blood Institute; American Heart Association; world heart federation; international atherosclerosis society; and International Association for the Study of obesity. Circulation 120 (16):1640–1645. doi:https://doi.org/10.1161/CIRCULATIONAHA.109.192644

  55. Rader DJ, Hovingh GK (2014) HDL and cardiovascular disease. Lancet 384(9943):618–625. https://doi.org/10.1016/S0140-6736(14)61217-4

    Article  CAS  PubMed  Google Scholar 

  56. Reiner Ž (2017) Hypertriglyceridaemia and risk of coronary artery disease. Nat Rev Cardiol 14(7):401–411. https://doi.org/10.1038/nrcardio.2017.31

    Article  CAS  PubMed  Google Scholar 

  57. Lagogianni I, Papapanagiotou A, Piperi C, Kalofoutis C, Troupis G, Zachari A, Kalofoutis A (2005) Evidence of reduced plasma HDL subfractions in patients with cutaneous discoid lupus erythematosus. Clin Biochem 38(3):286–290. https://doi.org/10.1016/j.clinbiochem.2004.10.006

    Article  CAS  PubMed  Google Scholar 

  58. Ambrose JA, Barua RS (2004) The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 43(10):1731–1737. https://doi.org/10.1016/j.jacc.2003.12.047

    Article  CAS  PubMed  Google Scholar 

  59. Price JF, Mowbray PI, Lee AJ, Rumley A, Lowe GD, Fowkes FG (1999) Relationship between smoking and cardiovascular risk factors in the development of peripheral arterial disease and coronary artery disease: Edinburgh artery study. Eur Heart J 20(5):344–353. https://doi.org/10.1053/euhj.1998.1194

    Article  CAS  PubMed  Google Scholar 

  60. Miot HA, Bartoli Miot LD, Haddad GR (2005) Association between discoid lupus erythematosus and cigarette smoking. Dermatology 211(2):118–122. https://doi.org/10.1159/000086440

    Article  PubMed  Google Scholar 

  61. Böckle BC, Sepp NT (2015) Smoking is highly associated with discoid lupus erythematosus and lupus erythematosus tumidus: analysis of 405 patients. Lupus 24(7):669–674. https://doi.org/10.1177/0961203314559630

    Article  PubMed  Google Scholar 

  62. Chasset F, Francès C, Barete S, Amoura Z, Arnaud L (2015) Influence of smoking on the efficacy of antimalarials in cutaneous lupus: a meta-analysis of the literature. J Am Acad Dermatol 72(4):634–639. https://doi.org/10.1016/j.jaad.2014.12.025

    Article  CAS  PubMed  Google Scholar 

  63. Gallego H, Crutchfield CE, Lewis EJ, Gallego HJ (1999) Report of an association between discoid lupus erythematosus and smoking. Cutis 63(4):231–234

    CAS  PubMed  Google Scholar 

  64. Klein R, Moghadam-Kia S, Taylor L, Coley C, Okawa J, LoMonico J, Chren MM, Werth VP (2011) Quality of life in cutaneous lupus erythematosus. J Am Acad Dermatol 64(5):849–858. https://doi.org/10.1016/j.jaad.2010.02.008

    Article  PubMed  PubMed Central  Google Scholar 

  65. Jalenques I, Rondepierre F, Massoubre C, Haffen E, Grand JP, Labeille B, Perrot JL, Aubin F, Skowron F, Mulliez A, D'Incan M, Group L (2016) High prevalence of psychiatric disorders in patients with skin-restricted lupus: a case-control study. Br J Dermatol 174(5):1051–1060. https://doi.org/10.1111/bjd.14392

    Article  Google Scholar 

  66. Rozanski A, Blumenthal JA, Kaplan J (1999) Impact of psychological factors on the pathogenesis of cardiovascular disease and implications for therapy. Circulation 99(16):2192–2217. https://doi.org/10.1161/01.cir.99.16.2192

    Article  CAS  PubMed  Google Scholar 

  67. Rozanski A, Blumenthal JA, Davidson KW, Saab PG, Kubzansky L (2005) The epidemiology, pathophysiology, and management of psychosocial risk factors in cardiac practice: the emerging field of behavioral cardiology. J Am Coll Cardiol 45(5):637–651. https://doi.org/10.1016/j.jacc.2004.12.005

    Article  PubMed  Google Scholar 

  68. Lesperance F, Frasure-Smith N, Talajic M, Bourassa MG (2002) Five-year risk of cardiac mortality in relation to initial severity and one-year changes in depression symptoms after myocardial infarction. Circulation 105(9):1049–1053. https://doi.org/10.1161/hc0902.104707

    Article  PubMed  Google Scholar 

  69. Jorge A, Lertratanakul A, Lee J, Pearce W, McPherson D, Thompson T, Barinas-Mitchell E, Ramsey-Goldman R (2017) Depression and progression of subclinical cardiovascular disease in systemic lupus Erythematosus. Arthritis Care Res (Hoboken) 69(1):5–11. https://doi.org/10.1002/acr.22992

    Article  Google Scholar 

  70. Grönhagen CM, Tang MB, Tan VW, Tan KW, Lim YL (2016) Vitamin D levels in 87 Asian patients with cutaneous lupus erythematosus: a case-control study. Clin Exp Dermatol 41(7):723–729. https://doi.org/10.1111/ced.12884

    Article  PubMed  Google Scholar 

  71. Heine G, Lahl A, Müller C, Worm M (2010) Vitamin D deficiency in patients with cutaneous lupus erythematosus is prevalent throughout the year. Br J Dermatol 163(4):863–865. https://doi.org/10.1111/j.1365-2133.2010.09948.x

    Article  CAS  PubMed  Google Scholar 

  72. Kendrick J, Targher G, Smits G, Chonchol M (2009) 25-Hydroxyvitamin D deficiency is independently associated with cardiovascular disease in the third National Health and nutrition examination survey. Atherosclerosis 205(1):255–260. https://doi.org/10.1016/j.atherosclerosis.2008.10.033

    Article  CAS  Google Scholar 

  73. Kim DH, Sabour S, Sagar UN, Adams S, Whellan DJ (2008) Prevalence of hypovitaminosis D in cardiovascular diseases (from the National Health and nutrition examination survey 2001 to 2004). Am J Cardiol 102(11):1540–1544. https://doi.org/10.1016/j.amjcard.2008.06.067

    Article  CAS  PubMed  Google Scholar 

  74. Martins D, Wolf M, Pan D, Zadshir A, Tareen N, Thadhani R, Felsenfeld A, Levine B, Mehrotra R, Norris K (2007) Prevalence of cardiovascular risk factors and the serum levels of 25-hydroxyvitamin D in the United States: data from the third National Health and nutrition examination survey. Arch Intern Med 167(11):1159–1165. https://doi.org/10.1001/archinte.167.11.1159

    Article  CAS  PubMed  Google Scholar 

  75. Lertratanakul A, Wu P, Dyer A, Urowitz M, Gladman D, Fortin P, Bae SC, Gordon C, Clarke A, Bernatsky S, Hanly JG, Isenberg D, Rahman A, Merrill J, Wallace DJ, Ginzler E, Khamashta M, Bruce I, Nived O, Sturfelt G, Steinsson K, Manzi S, Dooley MA, Kalunian K, Petri M, Aranow C, Font J, van Vollenhoven R, Stoll T, Ramsey-Goldman R (2014) 25-hydroxyvitamin D and cardiovascular disease in patients with systemic lupus erythematosus: data from a large international inception cohort. Arthritis Care Res (Hoboken) 66(8):1167–1176. https://doi.org/10.1002/acr.22291

    Article  CAS  Google Scholar 

  76. Wu PW, Rhew EY, Dyer AR, Dunlop DD, Langman CB, Price H, Sutton-Tyrrell K, McPherson DD, Edmundowicz D, Kondos GT, Ramsey-Goldman R (2009) 25-hydroxyvitamin D and cardiovascular risk factors in women with systemic lupus erythematosus. Arthritis Rheum 61(10):1387–1395. https://doi.org/10.1002/art.24785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Reynolds JA, Haque S, Berry JL, Pemberton P, Teh LS, Ho P, Gorodkin R, Bruce IN (2012) 25-Hydroxyvitamin D deficiency is associated with increased aortic stiffness in patients with systemic lupus erythematosus. Rheumatology (Oxford) 51(3):544–551. https://doi.org/10.1093/rheumatology/ker352

    Article  CAS  Google Scholar 

  78. Ravenell RL, Kamen DL, Spence JD, Hollis BW, Fleury TJ, Janech MG, Almeida JS, Shaftman SR, Oates JC (2012) Premature atherosclerosis is associated with hypovitaminosis D and angiotensin-converting enzyme inhibitor non-use in lupus patients. Am J Med Sci 344(4):268–273. https://doi.org/10.1097/MAJ.0b013e31823fa7d9

    Article  PubMed  PubMed Central  Google Scholar 

  79. Chang AY, Werth VP (2011) Treatment of cutaneous lupus. Curr Rheumatol Rep 13(4):300–307. https://doi.org/10.1007/s11926-011-0180-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Wu TK, Tsapogas MJ, Jordan FR (1977) Prophylaxis of deep venous thrombosis by hydroxychloroquine sulfate and heparin. Surg Gynecol Obstet 145(5):714–718

    CAS  PubMed  Google Scholar 

  81. Carter AE, Eban R (1974) Prevention of postoperative deep venous thrombosis in legs by orally administered hydroxychloroquine sulphate. Br Med J 3(5923):94–95. https://doi.org/10.1136/bmj.3.5923.94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Achuthan S, Ahluwalia J, Shafiq N, Bhalla A, Pareek A, Chandurkar N, Malhotra S (2015) Hydroxychloroquine's efficacy as an antiplatelet agent study in healthy volunteers: a proof of concept study. J Cardiovasc Pharmacol Ther 20(2):174–180. https://doi.org/10.1177/1074248414546324

    Article  CAS  PubMed  Google Scholar 

  83. Sharma TS, Wasko MC, Tang X, Vedamurthy D, Yan X, Cote J, Bili A (2016) Hydroxychloroquine use is associated with decreased incident cardiovascular events in rheumatoid arthritis patients. J Am Heart Assoc 5(1). https://doi.org/10.1161/JAHA.115.002867

  84. Fasano S, Pierro L, Pantano I, Iudici M, Valentini G (2017) Longterm Hydroxychloroquine therapy and low-dose aspirin may have an additive effectiveness in the primary prevention of cardiovascular events in patients with systemic lupus Erythematosus. J Rheumatol 44(7):1032–1038. https://doi.org/10.3899/jrheum.161351

    Article  CAS  PubMed  Google Scholar 

  85. Sholter DE, Armstrong PW (2000) Adverse effects of corticosteroids on the cardiovascular system. Can J Cardiol 16(4):505–511

    CAS  PubMed  Google Scholar 

  86. Chen M, Doherty SD, Hsu S (2010) Innovative uses of thalidomide. Dermatol Clin 28(3):577–586. https://doi.org/10.1016/j.det.2010.03.003

    Article  CAS  PubMed  Google Scholar 

  87. Fabi SG, Hill C, Witherspoon JN, Boone SL, West DP (2009) Frequency of thromboembolic events associated with thalidomide in the non-cancer setting: a case report and review of the literature. J Drugs Dermatol 8(8):765–769

    PubMed  Google Scholar 

  88. Durosaro O, Davis MD, Reed KB, Rohlinger AL (2009) Incidence of cutaneous lupus erythematosus, 1965-2005: a population-based study. Arch Dermatol 145(3):249–253. https://doi.org/10.1001/archdermatol.2009.21

    Article  PubMed  PubMed Central  Google Scholar 

  89. Hu SC, Lan CE (2017) Psoriasis and cardiovascular comorbidities: focusing on severe vascular events, cardiovascular risk factors and implications for treatment. Int J Mol Sci 18(10). https://doi.org/10.3390/ijms18102211

  90. Churton S, Brown L, Shin TM, Korman NJ (2014) Does treatment of psoriasis reduce the risk of cardiovascular disease? Drugs 74(2):169–182. https://doi.org/10.1007/s40265-013-0173-5

    Article  CAS  PubMed  Google Scholar 

  91. Yang ZS, Lin NN, Li L, Li Y (2016) The effect of TNF inhibitors on cardiovascular events in psoriasis and psoriatic arthritis: an updated meta-analysis. Clin Rev Allergy Immunol 51(2):240–247. https://doi.org/10.1007/s12016-016-8560-9

    Article  CAS  PubMed  Google Scholar 

  92. Jacobsson LT, Turesson C, Gülfe A, Kapetanovic MC, Petersson IF, Saxne T, Geborek P (2005) Treatment with tumor necrosis factor blockers is associated with a lower incidence of first cardiovascular events in patients with rheumatoid arthritis. J Rheumatol 32(7):1213–1218

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vinod E. Nambudiri.

Ethics declarations

Disclosures

None.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Code availability

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, L.N., Nambudiri, V.E. Cutaneous lupus erythematosus and cardiovascular disease: current knowledge and insights into pathogenesis. Clin Rheumatol 40, 491–499 (2021). https://doi.org/10.1007/s10067-020-05257-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-020-05257-3

Keywords

Navigation