Lviv clinical bulletin 2021, 1(33)-2(34): 37-50

https://doi.org/10.25040/lkv2021.01-02.037

Modern View on the Problem of Systemic Lupus Erythematosus with and without Comorbid Lesions of the Circulatory System (Literature Review, Clinical Case Description) (first notice)

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L. Kobak, O. Abrahamovych, U. Abrahamovych, V. Chemes

Danylo Halytsky Lviv National Medical University

Context. The prevalence and incidence of systemic lupus erythematosus (SLE) in the world is significant. In recent years, there has been a tendency of the SLE prevalence increase. despite the undoubted progress in understanding the etiology and pathogenesis of SLE, its diagnosis and treatment, the mortality of patients, including ones at young and working age, is higher than in the general population, and circulatory system lesions are ones of its main reasons in these cases.

Objective. To analyze the literature, dedicated to the modern view on the problem of systemic lupus erythematosus with and without comorbid lesions of the circulatory system, describe the clinical case.

Materials and methods. Content analysis, method of system and comparative analysis, bibliosemantic method of studying the current scientific investigations on modern principles of diagnosis and treatment of patients with SLE are used. A clinical case is described.

Results. The article presents modern ideas about the etiological factors and pathogenesis of the disease. The clinical manifestations of SLE are very diverse. The problem of comorbidity and syntropy of lesions is relevant. Lesions of the cardiovascular system in the case of SLE can manifest itself in the form of pericarditis, myocarditis, endocarditis, lesions of the heart valves, coronary arteries, aorta, conduction system, pulmonary hypertension occurrence. The basic principles of drug therapy are also briefly considered.

Conclusions. The results of the literature review indicate the importance of the problem of systemic lupus erythematosus, due to its widespread prevalence among the young and people of working age, lack of accurate knowledge about the etiology and pathogenesis of the disease, comorbid lesions of many organs and systems, including circulatory system, the development of severe and often life-threatening manifestations, the lack of clear recommendations that would predict the differentiated use of drugs taking into account comorbid syntropic lesions, which is also demonstrated in the described clinical case. Given this, systemic lupus erythematosus needs further in-depth study.

References

  1. Abrahamovych O, Abrahamovych U, Guta S, Farmaha M, Kobak L. Cytomegalovirus and Virus Epstein-Barr Infection in Patients With Systemic Lupus Erythematosus and Its Dependence on Gender and Age of Patients. World Sci. 2020;8(60):0-6 (Ukrainian) https://doi.org/10.31435/rsglobal_ws/31102020/7225
  2. Abrahamovych О, Abrahamovych U, Kushyna A, Guta S, Farmaha M. Dependence of heart rate іn terms of the daіly monіtorіng іndіcators on the actіvіty of pathologіcal process іn patіents wіth systemіc lupus erythematosus Georgіan Medіcal News. 2016;10(259):53-57 (Ukrainian)
  3. Abrahamovych О, Abrahamovych U, Kushyna A, Guta S, Synenkyi O. Dependence of Indicators of Daily Blood Pressure Monitoring on Activity of Pathological Process in Patients with Systemic Lupus Erythematosus. Lviv clinical bulletin. 2016;2(14)-3(15):14-22 (Ukrainian) https://doi.org/10.25040/lkv2016.023.014
  4. Abrahamovych O, Fayura O, Abrahamovych U. Comorbidity: a Modern View on the Problem; Classification (first notice). Lviv clinical bulletin. 2015;4(12):56-64 (Ukrainian) https://doi.org/10.25040/lkv2015.04.056
  5. Abrahamovych O, Fayura O, Abrahamovych U. Comorbidity: a Modern View on the Problem; Classification (second notice). Lviv clinical bulletin. 2016;1(13):31-39 (Ukrainian) https://doi.org/10.25040/lkv2016.01.031
  6. Abrahamovych U, Abrahamovych O, Nadashkevich O, Farmaha M, Kobak L. Pathogenetic Association of Digestive System Lesions with Systemic Lupus Erythematosus: Characteristics and Prevalence. Psychosom Med Gen Pract. 2020;5(1):e0501225 (Ukrainian) https://doi.org/10.26766/pmgp.v5i1.225
  7. Abrahamovych UO, Abrahamovych OO, Farmaha ML, Romaniuk OT, Kobak LO. Pаthogenetic association of vascular and cardiac lesions with systemic lupus erythematosus: charasteristics and prevalence. Art of Medicine. 2020;2(14):6-15 (Ukrainian) https://doi.org/10.21802/artm.2020.2.14.6.
  8. Ajeganova S, Gustafsson T, Jogestrand T. Bone mineral density and carotid atherosclerosis in systemic lupus erythematosus: a controlled cross-sectional study. Arthritis Res. Ther. 2015;17(1):84. https://doi.org/10.1186/s13075-015-0595-4
  9. Al Rayes H, Harvey PJ, Gladman DD, Su J, Sabapathy A, Urowitz MB, Touma Z. Prevalence and associated factors of resting electrocardiogram abnormalities among systemic lupus erythematosus patients without cardiovascular disease. Arthritis Research & Therapy. 2017;19:31. https://doi.org/10.1186/s13075-017-1240-1
  10. Amosova KM, Yaremenko OB, Matiyashchuk IG. Traditional and specific risk factors of atherosclerosis in patients with systemic lupus erythematosus. Ukrainian Journal of Rheumatology. 2012;1:5-11 (Ukrainian)
  11. An J, Minie M, Sasaki T. Antimalarial Drugs as Immune Modulators: New Mechanisms for Old Drugs. Annu Rev. Med. 2017;68:317-330. https://doi.org/10.1146/annurev-med-043015-123453
  12. Andreoli L, Bertsias GK, Agmon-Levin N. EULAR recommendations for women’s health and the management of family planning, assisted reproduction, pregnancy and menopause in patients with systemic lupus erythematosus and/or antiphospholipid syndrome. Ann. Rheum. Dis. 2016. https://doi.org/10.1136/annrheumdis-2016-209770
  13. Angel A, Justiz V, Amandeep G et al. Systemic Lupus Erythematosus (SLE). StatPearls Publishing, Treasure Island (FL), 2020 Jan.
  14. Apostolopoulos D, Kandane-Rathnayake R, Raghunath S. Independent association of glucocorticoids with damage accrual in SLE. Lupus Sci Med. 2016;3:e000157. https://doi.org/10.1136/lupus-2016-000157
  15. Aringer M, Costenbader K, Daikh D et al. European League Against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus. Ann Rheum Dis. 2019;78(9):1151-1159.
  16. Aringer M, Dorner T, Leuchten N, Johnson SR. Toward new criteria for systemic lupus erythematosus – a standpoint. Lupus. 2016;25:805-811. https://doi.org/10.1177/0961203316644338
  17. Aringer M, Schneider M. Management of systemic lupus erythematosus. Internist (Berl). 2016;57(11):1052-1059. https://doi.org/10.1007/s00108-016-0135-6
  18. Artola RT, Mihos CG, Santana O. Effects of Statin Therapy in Patients with Systemic Lupus Erythematosus. South Med. J. 2016;109(11):705-711.
  19. Azrielant S, Tiosano S, Watad A. Correlation between systemic lupus erythematosus and malignancies: a cross-sectional population-based study. Immunol Res. 2017;1-6. https://doi.org/10.1007/s12026-016-8885-8
  20. Bani Hani A, Abu-Abeeleh M, Al Kharabsheh MM, Qabba’ah L. Libman-Sacks Endocarditis with Unusual Large Size Vegetation Involving the Mitral Valve. Heart Surg Forum. 2016;19(6):E294-E296. https://doi.org/10.1532/hsf.1612
  21. Belibou C, Ancuta C, Ancuta E, Filos C, Chirieac R. Carotid intima-media thickness and plaque as surrogate biomarkers of atherosclerosis amond consecutive women with systemic lupus erythematosus. Rom J Morphol Embryol. 2012;53(1):29-34.
  22. Beloglazov VA, Shaduro DV, Gordienko AI, Bakova AA. Imbalance of the humoral link of antiendotoxin immunity and its influence on systemic inflammation, endogenous intoxication in patients with systemic lupus erythematosus. Immunology and Allergy: Science and Practice. 2014;2:45-51 (Ukrainian)
  23. Beregniy V, Marushko T, Marushko I. Characteristic of cardiac lesion in patients with systemic lupus erythematosus. Modern Pediatrics. 2010;6(34):128-131 (Ukrainian)
  24. Binello N, Cancelli C, Passalacqua S et al. Use of Intravenous Immunoglobulin Therapy at Unconventional Doses in Refractory Fulminant Systemic Lupus Erythematosus. Eur J Case Rep Intern Med. 2018;5(9):000934. https://doi.org/10.12890/2018_000934
  25. Bogmat LF, Shevchenko NS, Matvienko EV. Use of SLICC/ACR damage index in adolescent with SLE. Ukrainian Journal of Rheumatology. 2015;2:42-45 (Ukrainian)
  26. Bourré-Tessier J, Urowitz MB, Clarke AE, Bernatsky S, Krantz MJ, Huynh T et al. Electrocardiographic findings in systemic lupus erythematosus: data from an international inception cohort. Arthritis Care Res (Hoboken). 2014;67(1):128-135. https://doi.org/10.1002/acr.22370
  27. Chakravarty EF. Incidence and Prevention of Herpes Zoster Reactivation in Patients with Autoimmune Diseases. Rheum Dis Clin North Am. 2017;43(1):111-121. https://doi.org/10.1016/j.rdc.2016.09.010
  28. Cheetham TC, Marcy SM, Tseng H, Sy LS, Liu IA, Bixler F et al. Risk of herpes zoster and disseminated varicella zoster in patients taking immunosuppressant drugs at the time of zoster vaccination. Mayo Clin Proc. 2015;90(7):865-873. https://doi.org/10.1016/j.mayocp.2015.04.021
  29. Chen HL, Shen L-J, Hsu P-N et al. Cumulative Burden of Glucocorticoid-related Adverse Events in Patients with Systemic Lupus Erythematosus: Findings from a 12-year Longitudinal Study. J Rheumatol. 2018;45(1):83-89. https://doi.org/10.3899/jrheum.160214
  30. Choi MY, Clarke AE, St Pierre Y, Hanly JG, Urowitz MB, Romero-Diaz J et al. Antinuclear Antibody-Negative Systemic Lupus Erythematosus in an International Inception Cohort. Arthritis Care Res (Hoboken). 2019;71(7):893-902. https://doi.org/10.1002/acr.23712
  31. Christou EAA, Banos A, Kosmara D et al. Sexual dimorphism in SLE: above and beyond sex hormones. Lupus. 2019;28(1):3-10. https://doi.org/10.1177/0961203318815768
  32. Dall’Ara F, Andreoli L, Piva N. Winter lupus flares are associated with low vitamin D levels in a retrospective longitudinal study of Italian adult patients. Clin Exp Rheumatol. 2015;33(2):153-158.
  33. Di Virgilio F, Giuliani AL. Purinergic signalling in autoimmunity: A role for the P2X7R in systemic lupus erythematosus? Biomed J. 2016;39(5):326-338. https://doi.org/10.1016/j.bj.2016.08.006
  34. Dolcino M, Puccetti A, Barbieri A, Bason C, Tinazzi E, Ottria A et al. Infections and autoimmunity: role of human cytomegalovirus in autoimmune endothelial cell damage. Lupus. 2015;24:419-432. https://doi.org/10.1177/0961203314558677
  35. Domingues V, Magder LS, Petri M. Assessment of the independent associations of IgG, IgM and IgA isotypes of anticardiolipin with thrombosis in SLE. Lupus Sci Med. 2016;3:126-131. https://doi.org/10.1136/lupus-2015-000107
  36. Eder L, Gladman DD, Ibañez D, Urowitz MB. The correlation between carotid artery atherosclerosis and clinical ischemic heart disease in lupus patients. Lupus. 2014;23(11):1142-1148.
    https://doi.org/10.1177/0961203314537696
  37. Elnady BM, Abdelghafar AS, Khalik ES. The implication of tissue Doppler echocardiography and cardiopulmonary exercise in early detection of cardiac dysfunction in systemic lupus erythematosus patients. Eur J Rheumatol. 2016;3(3):109-117. https://doi.org/10.5152/eurjrheum.2016.16002
  38. Fanouriakis A, Kostopoulou M, Alunno A et al. 2019 update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis. 2019;78:36-745. https://doi.org/10.1136/annrheumdis-2019-215089
  39. Fanouriakis A, Kostopoulou M, Cheema K et al. 2019 Update of the Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of lupus nephritis. Ann Rheum Dis. 2020;79(6):713-723. https://doi.org/10.1136/rmdopen-2020-001263
  40. Finzel S, Schaffer S, Rizzi M et al. Pathogenese des systemischen Lupus erythematodes [Pathogenesis of systemic lupus erythematosus]. Z Rheumatol. 2018;77(9):789-798. https://doi.org/10.1007/s00393-018-0541-3
  41. Frieri M, Stampfl H. Systemic lupus erythematosus and atherosclerosis: Review of the literature. Autoimmun Rev. 2016;15(1):16-21. https://doi.org/10.1016/j.autrev.2015.08.007
  42. Fujiwara S, Takei M. Epstein-Barr virus and autoimmune diseases. Clin Exp Neuroimmunol. 2015;6(1):38-48. https://doi.org/10.1111/cen3.12263
  43. Garcia-Carrasco M, Romero-Galvez JL. Vitamin D and cardiovascular disease in patients with systemic lupus erythematosus. Reumatol Clin. 2016;12:241-243. https://doi.org/10.1016/j.reumae.2016.07.003
  44. García-Villegas EA, Márquez-González H, Flores-Suárez LF, Villa-Romero AR. The pulse-mass index as a predictor of cardiovascular events in women with systemic lupus erythematosus. Med Clin (Barc). 2017;148(2):57-62. https://doi.org/10.1016/j.medcli.2016.09.017
  45. Gergianaki I, Bertsias G. Systemic Lupus Erythematosus in Primary Care: An Update and Practical Messages for the General Practitioner. Front Med (Lausanne). 2018;5:161. https://doi.org/10.3389/fmed.2018.00161
  46. Gomez Mendez LM, Cascino MD, Garg J et al. Peripheral Blood B Cell Depletion after Rituximab and Complete Response in Lupus Nephritis. Clin J Am Soc Nephrol. 2018;13(10):1502-1509. https://doi.org/10.2215/CJN.01070118
  47. Gustafsson J. Studies on cardiovascular risk factors in Systemic Lupus Erythematosus. Stockholm: Karolinska Institutet; 2012. 71 p.
  48. Guy A, Tiosano S, Comaneshter D. Aortic aneurysm association with SLE – a case-control study. Lupus. 2016;25(9):959-963. https://doi.org/10.1177/0961203316628999
  49. Haładyj E, Paradowska-Gorycka A, Felis-Giemza A, Olesińska M. Immunity and early atherosclerosis in the course of systemic lupus erythematosus, mixed connective tissue disease and antiphospholipid syndrome. Reumatologia. 2016;54(4):187-195. https://doi.org/10.5114/reum.2016.62473
  50. Han GM, Han XF. Comorbid Conditions are Associated With Emergency Department Visits, Hospitalizations, and Medical Charges of Patients With Systemic Lupus Erythematosus. J Clin Rheumatol. 2017;23(1):19-25. https://doi.org/10.1097/RHU.0000000000000437
  51. Hatef-Fard MR, Khodabandeh M, Sahebari M. Metabolic syndrome in lupus patients in northeast of Iran, and their lifestyle habits. Caspian J Intern Med. 2016;7(3):195-200.
  52. He Y, Huang Y, Tu L. Decreased Gαq expression in T cells correlates with enhanced cytokine production and disease activity in systemic lupus erythematosus. Oncotarget. 2016;7(52):85741-85749. https://doi.org/10.18632/oncotarget.13903
  53. He Y, Sawalha AH. Drug-induced lupus erythematosus: an update on drugs and mechanisms. Curr Opin Rheumatol. 2018;30(5):490-497. https://doi.org/10.1097/BOR.0000000000000522
  54. Hermansen ML, Lindhardsen J, Torp-Pedersen C. The risk of cardiovascular morbidity and cardiovascular mortality in systemic lupus erythematosus and lupus nephritis: a Danish nationwide population-based cohort study. Rheumatology (Oxford). 2017;56(5):709-715. https://doi.org/10.1093/rheumatology/kew475
  55. Herrinton LJ, Liu L, Goldfien R, Michaels MA, Tran TN. Risk of serious infection for patients with systemic lupus erythematosus starting glucocоrticoids with or without antimalarials. J Rheumatol. 2016;43:1503-1509. https://doi.org/10.3899/jrheum.150671
  56. Heshmat TS, Khalil NM, Elhamid HA, Labib S, Mahfouz M. Assessment of premature coronary atherosclerosis in patients with systemic lupus erythematosus disease. Egyptian Rheumatologist. 2015;37:43-47. https://doi.org/10.1016/j.ejr.2015.04.001
  57. Hsu CY, Lin M-S, SuYu-J et al. Cumulative immunosuppressant exposure is associated with diversified cancer risk among 14 832 patients with systemic lupus erythematosus: a nested case-control study. Rheumatol (Oxford). 2017;56:620-628. https://doi.org/10.1093/rheumatology/kex255
  58. Iaccarino L, Andreoli L, Bartoloni Boc E et al. Clinical predictors of response and discontinuation of belimumab in patients with systemic lupus erythematosus in real life setting. Results of a large, multicentric, nationwide study. J Autoimmun. 2018;86:1-8. https://doi.org/10.1016/j.jaut.2017.09.004
  59. Justiz Vaillant AA, Goyal A, Bansal P et al. Systemic Lupus Erythematosus (SLE). StatPearls Publishing, Treasure Island (FL), 2020 Jan.
  60. Ju-Yang Jung, Chang-Hee Suh. Infection in systemic lupus erythematosus, similarities, and differences with lupus flare. Korean J Intern Med. 2017;32(3):429-438. https://doi.org/10.3904/kjim.2016.234
  61. Kay SD, Poulsen MK, Diederichsen AC, Voss A. Coronary, Carotid, and Lower-extremity Atherosclerosis and Their Interrelationship in Danish Patients with Systemic Lupus Erythematosus. J Rheumatol. 2016;43(2):315-322. https://doi.org/10.3899/jrheum.150488
  62. Keeling SO, Alabdurubalnabi Z, Avina-Zubieta A, Barr S, Bergeron L, Bernatsky S et al. Canadian Rheumatology Association Recommendations for the Assessment and Monitoring of Systemic Lupus Erythematosus. J Rheumatol. 2018;45(9):1340-1355. https://doi.org/10.3899/jrheum.171459
  63. Khairy N, Ezzat Y, Naeem N, Taha R, Wesam R. Atherosclerosis biomarkers in female systemic lupus erythematosus patients with and without cardiovascular diseases. Egyptian Rheumatologist. 2017;39:7-12. https://doi.org/10.1016/j.ejr.2016.03.003
  64. Kiani AN, Aukrust P, Ueland T, Hollan I, Barr E, Magder LS, Petri M. Serum osteoprotegеrin (OPG) in subclinical atherosclerosis in systemic lupus erythematosus. Lupus. 2017;26(8):865-870. https://doi.org/10.1177/0961203316682101
  65. Kim CH, Al-Kindi SG, Jandali B. Incidence and risk of heart failure in systemic lupus erythematosus. Heart. 2017;103(3):227-233. https://doi.org/10.1136/heartjnl-2016-309561
  66. Kim D, Choi J, Cho SK. Clinical characteristics and outcomes of diffuse alveolar hemorrhage in patients with systemic lupus erythematosus. Semin Arthritis Rheum. 2017;46(6):782-787. https://doi.org/10.1016/j.semarthrit.2016.09.004
  67. Klyukvina NG. Systemic lupus erythematosus and vitamin D. Modern Rheumatology. 2015;9(2):57-65 (Russian) https://doi.org/10.14412/1996-7012-2015-2-57-65
  68. Kovalenko VM, Kornatsky VM, editor. Stress and cardiovascular diseases. Kyiv: State Institution “National Research Center” Institute of Cardiology named after Acad. Strazchesko MD»; 2015. 356 p. (Ukrainian)
  69. Kovalenko VM, Kornatsky VM. The health of the people of Ukraine and tertiary health care: a guide. K.: SI NSC Institute of Cardiology named after Acad. Strazchesko MD; 2019. 193 p. (Ukrainian)
  70. Kovalenko VM, Rekalov DG, Yatsyshyn RI at al. Systemic lupus erythematosus (clinical guidelines). K.: Ukrainian Association of Rheumatologists; 2020. 74 p. (Ukrainian)
  71. Kovalenko VN, Gnilorybov AM, Ter-Vartanian CH, Yaremenko ОB. 2014 EULAR Congress (Paris, 11-14 June): the review of congress materials. Ukrainian Journal of Rheumatology. 2014;4:11-20 (Ukrainian)
  72. Kovalenko VN, Golovach IYu, Bortkevych OP. Achievements treatment of systemic lupus erythematosus. Ukrainian Journal of Rheumatology. 2012;50(4):16-22 (Ukrainian)
  73. Kuchinskaya EM, Suspitsyn EN, Kostik MM. Genetic aspects of the pathogenesis of systemic lupus erythematosus in children. Modern Rheumatology. 2020;14(1):101-107 (Russian) https://doi.org/10.14412/1996-7012-2020-1-101-107
  74. Kurien BT, Fesmire J, Anderson CJ, Scofield RH. Anti-Ro and Concomitant Anti-La Autoantibodies Strongly Associated With Anti-oxLDL or Anti-Phospholipid Antibody in Systemic Lupus Erythematosus. J Clin Rheumatol. 2016;22(8):418-425. https://doi.org/10.1097/RHU.0000000000000429
  75. Lam NC, Ghetu MV, Bieniek ML. Systemic Lupus Erythematosus: Primary Care Approach to Diagnosis and Management. Am Fam Physician. 2016;94(4):284-294.
  76. Langkilde H, Voss A, Heegaard N, Laustrup H. Autoantibodies persist in relatives to systemic lupus erythematosus patients during 12 years follow-up. Lupus. 2017;26(7):723-728. https://doi.org/10.1177/0961203316676378
  77. Larosa M, Iaccarino L, Gatto M. Advances in the diagnosis and classification of systemic lupus erythematosus. Exp Rev Clin Immunol. 2016;12(12):1309-1320. https://doi.org/10.1080/1744666X.2016.1206470
  78. Lewandowski LB, Kaplan MJ. Update on cardiovascular disease in lupus. Curr Opin Rheumatol. 2016;28(5):468-476. https://doi.org/10.1097/BOR.0000000000000307
  79. Lewis MJ, Jawad AS. The effect of ethnicity and genetic ancestry on the epidemiology, clinical features and outcome of systemic lupus erythematosus. Rheumatology (Oxford). 2016;56:67-77. https://doi.org/10.1093/rheumatology/kew399
  80. Li S, Liu S, Chen F. Link-Polymorphism of 5-HTT Promoter Region Is Associated with Autoantibodies in Patients with Systemic Lupus Erythematosus. J Immunol Res. 2016;2016:1-6. https://doi.org/10.1155/2016/3042726
  81. Lila VA. Clinical and laboratory relationships in patients with different variants of systemic lupus erythematosus. Modern rheumatology. 2020;14(1):26-31 (Russian) https://doi.org/10.14412/1996-7012-2020-1-26-31
  82. Little J, Parker B, Lunt M, Hanly JG, Urowitz MB, Clarke AE, et al. Glucocorticoid use and factors associated with variability in this use in the Systemic Lupus International Collaborating Clinics Inception Cohort Rheumatology (Oxford, England). 2018;57(4):677-687.
  83. Liu Y, Cui Y, Zhang X, Gao X, Su Y, Xu B. Effects of salvianolate on bone metabolism in glucocorticoid-treated lupus-prone B6.MRL-Faslpr/J mice. Drug Des Devel Ther. 2016;10:2535-2546. https://doi.org/10.2147/DDDT.S110125
  84. Lo MS, Tsokos GC. Recent developments in systemic lupus erythematosus pathogenesis and applications for therapy. Curr Opin Rheumatol. 2018;30(2):222-228. https://doi.org/10.1097/BOR.0000000000000474
  85. Lood C, Tydén H, Gullstrand B. Decreased platelet size is associated with platelet activation and anti-phospholipid syndrome in systemic lupus erythematosus. Rheumatology (Oxford). 2017;56(3):408-416. https://doi.org/10.1093/rheumatology/kex216
  86. Louthrenoo W. Treatment considerations in patients with concomitant viral infection and autoimmune rheumatic diseases. Best Pract Res Clin Rheumatol. 2015;29(2):319-342. https://doi.org/10.1016/j.berh.2015.05.010
  87. Macedo ACL, Isaac L. Systemic Lupus Erythematosus and Deficiencies of Early Components of the Complement Classical Pathway. Front Immunol. 2016;7:55. https://doi.org/10.3389/fimmu.2016.00055
  88. Mackay M, Oswald M, Sanchez-Guerrero J, Lichauco J, Aranow C, Kotkin S, et al. Molecular signatures in systemic lupus erythematosus: distinction between disease flare and infection. Lupus Sci Med. 2016;3:1-10. https://doi.org/10.1136/lupus-2016-000159
  89. Marushko EY. Clinical, immunological and morphofunctional characteristics of the cardiovascular system in children with juvenile rheumatoid arthritis and systemic lupus erythematosus [dissertation]. K.: National Academy of Medical Sciences of Ukraine, Institute of Pediatrics, Obstetrics and Gynecology; 2014. 24 р. (Ukrainian)
  90. Medeiros MM, de Oliveira IMX, Ribeiro AT. Prevalence of metabolic syndrome in a cohort of systemic lupus erythematosus patients from Northeastern Brazil: association with disease activity, nephritis, smoking, and age. Rheumatol Int. 2016;36(1):117-124. https://doi.org/10.1007/s00296-015-3316-z
  91. Mirfeizi Z, Poorzand H, Javanbakht A, Khajedaluee M. Relationship Between Systemic Lupus Erythematosus Disease Activity Index Scores and Subclinical Cardiac Problems. Iran Red Crescent Med J. 2016;18(8):e38045. https://doi.org/10.5812/ircmj.38045
  92. Mok CC, Ying SKY, Ma KM, Wong CK. Effect of raloxifene on disease activity and vascular biomarkers in patients with systemic lupus erythematosus: Subgroup analysis of a double-blind randomized controlled trial. Lupus. 2013;22:1470-1478. https://doi.org/10.1177/0961203313507987
  93. Moya FB, Pineda Galindo LF, García de la Pena M. Impact of Chronic Glucocorticoid Treatment on Cardiovascular Risk Profile in Patients with Systemic Lupus Erythematosus. J Clin Rheumatol. 2016;22(1):8-12. https://doi.org/10.1097/RHU.0000000000000335
  94. Mukvich OM, Omelchenko LI, Belska OA, Dudka IV, Ludvik TA, Matskevich AM. Complex issues of early diagnosis of systemic lupus erythematosus in children. The Health of the Child. 2020;15(2):112-119 (Ukrainian) https://doi.org/10.22141/2224-0551.15.2.2020.200274
  95. Munoz-Grajales C, Gonzalez LA, Alarcon GS, Acosta-Reyes J. Gender differences in disease activity and clinical features in newly diagnosed systemic lupus erythematosus patients. Lupus. 2016;25:1217-1223. https://doi.org/10.1177/0961203316635286
  96. Murdaca G, Orsi A, Spano F, Faccio V, Puppo F, Durando P, et al. Vaccine-preventable infections in systemic lupus erythematosus. Hum Vaccin Immunother. 2016;12(3):632-643. https://doi.org/10.1080/21645515.2015.1107685
  97. Mykhailovskaya NS, Shevchenko IO, Zelenina OA. Pathogenetic relationship between coronary heart disease and osteopenic syndrome. Zaporozhye Medical Journal. 2015;1:105-110 (Ukrainian) https://doi.org/10.14739/2310-1210.2015.1.39876
  98. Nascif AK, Hilario MO, Terreri MT. Endothelial function analysis and atherosclerotic rick factors in adolescents with systemic lupus erythematosus. Int J Adolesc Med Health. 2007;19(4):497-505. https://doi.org/10.1515/IJAMH.2007.19.4.497
  99. Neto NSR, Muniz LF, Costa LP. Herpes Zoster Ophthalmicus in a Patient with Systemic Lupus Erythematosus and Antiphospholipid Syndrome. Turk J Rheumatol. 2012;27(4):273-274. https://doi.org/10.5606/tjr.2012.050
  100. Ngaіdé AA, Ly F, Ly K. Cardiovascular manifestations in systemic lupus erythematosus in Dakar: Descriptive study about 50 cases. Bull Soc Pathol Exot. 2016;109(5):345-352. https://doi.org/10.1007/s13149-016-0529-7
  101. Nikpour M, Gladman DD, Urowitz MB. Premature coronary heart disease in systemic lupus erythematosus: what risk factor do we understand? Lupus. 2013;22:1243-1250. https://doi.org/10.1177/0961203313493031
  102. Nossent JC, Raymond WD, Eilertsen GO. Increased von Willebrand factor levels in patients with systemic lupus erythematosus reflect inflammation rather than increased propensity for platelet activation. Lupus Sci Med. 2016;3:e000162. https://doi.org/10.1136/lupus-2016-000162
  103. Olesińska M, Saletra A. Quality of life in systemic lupus erythematosus and its measurement. Reumatol. 2018;56(1):45-54. https://doi.org/10.5114/reum.2018.74750
  104. Pakchotanon R, Gladman DD, Su J, Urowitz MB. More Consistent Antimalarial Intake in First 5 Years of Disease Is Associated with Better Prognosis in Patients with Systemic Lupus Erythematosus. J Rheumatol. 2018;45(1):90-94. https://doi.org/10.3899/jrheum.170645
  105. Panchal L, Divate S, Vaideeswar P. Cardiovascular involvement in systemic lupus erythematosus: an autopsy study of 27 patients in India. J Postgrad Med. 2006;52:5-10.
  106. Paradowska-Gorycka A, Felis-Giemza A, Olesińska M, Haładyj E. Immunity and early atherosclerosis in the course of systemic lupus erythematosus, mixed connective tissue disease and antiphospholipid syndrome. Reumatologia. 2016;54(4):187-195. https://doi.org/10.5114/reum.2016.62473
  107. Park JK, Kim JY, Moon JY. Altered lipoproteins in patients with systemic lupus erythematosus are associated with augmented oxidative stress: a potential role in atherosclerosis. Arthritis Res Ther. 2016;18(1):306. https://doi.org/10.1186/s13075-016-1204-x
  108. Pérez-Sánchez C, Aguirre MA, Ruiz-Limón P. Atherothrombosis-associated microRNAs in Antiphospholipid syndrome and Systemic Lupus Erythematosus patients. Sci Rep. 2016;6:31375. https://doi.org/10.1038/srep31375
  109. Petrі M. Use of hydroxychloroquine to prevent thrombosis in systemic lupus erythematosus and in antiphospholipid antibody-positive patients. Curr Rheumatol Rep. 2011;13:77-80. https://doi.org/10.1007/s11926-010-0141-y
  110. Protsenko GO, Dubas VV. Systemic lupus erythematosus: the state of the problem in Ukraine and the world. Ukrainian Journal of Rheumatology. 2020;4(82):25-34 (Ukrainian)
  111. Rees F, Doherty M, Grainge MJ et al. The worldwide incidence and prevalence of systemic lupus erythematosus: a systematic review of epidemiological studies. Rheumatol (Oxford). 2017;56(11):1945-1961. https://doi.org/10.1093/rheumatology/kex260
  112. Rentero ML, Amigo E, Chozas N et al. Prevalence of fractures in women with rheumatoid arthritis and/or systemic lupus erythematosus on chronic glucocorticoid therapy. BMC Musculoskelet. Disord. 2015;16:300. https://doi.org/10.1186/s12891-015-0733-9
  113. Rigante D, Esposito S. Infections and Systemic Lupus Erythematosus: Binding or Sparring Partners? Int J Mol Sci. 2015;(16):17331-17343. https://doi.org/10.3390/ijms160817331
  114. Robert J Lahita. Systemic lupus erythematosus. 4th edition. Elsevier Inc.; 2004. 913-942 р. https://doi.org/10.1016/B9-78-012433-9/01950-034X
  115. Rodríguez Huerta MD, Trujillo-Martín MM, Rúa-Figueroa Í et al. Healthy lifestyle habits for patients with systemic lupus erythematosus: A systemic review. Semin Arthritis Rheum. 2016;45(4):463-470. https://doi.org/10.1016/j.semarthrit.2015.09.003
  116. Romero-Díaz J, Acosta-Hernández RI, Criales-Vera S, Kimura-Hayama E, Domínguez-Quintana M, Morán-Contla R et al. Asymptomatic Coronary Artery Calcifications in Men with Systemic Lupus Erythematosus. J Rheumatol. 2018;45(5):663-670. https://doi.org/10.3899/jrheum.170330
  117. Romero-Diaz J, Vargas-Vorackova F, Kimura-Hayama E, Cortazar-Benitez LF, Gijon-Mitre R, Criales S et al. Systemic lupus erythematosus risk factors for coronary artery calcifications. Rheumatology. 2012;51:110-119. https://doi.org/10.1093/rheumatology/ker307
  118. Ruiz-Arruza I, Ugarte A, Cabezas-Rodriguez I et al. Glucocorticoids and irreversible damage in patients with systemic lupus erythematosus. Rheumatology (Oxford). 2014;53(8):1470-1476. https://doi.org/10.1093/rheumatology/keu148
  119. Sacre K, Escoubet B, Zennaro MC. Overweight Is a Major Contributor to Atherosclerosis in Systemic Lupus Erythematosus Patients at Apparent Low Risk for Cardiovascular Disease: A Cross-Sectional Controlled Study. Medicine (Baltimore). 2015;94(48):e2177. https://doi.org/10.1097/MD.0000000000002177
  120. Sakir GY, Atılgan CU, Tekin K et al. Validity of Optical Coherence Tomography Angiography as a Screening Test for the Early Detection of Retinal Changes in Patients with Hydroxychloroquine Therapy. J Curr Eye Res. 2019;44(3):311-315. https://doi.org/10.1080/02713683.2018.1545912
  121. Santos EC, Pinto AC, Klumb EM, Macedo JM. Polymorphisms in NAT2 (N-acetyltransferase 2) gene in patients with systemic lupus erythematosus. Rev Bras Reumatol Engl Ed. 2016;56(6):521-529. https://doi.org/10.1016/j.rbr.2016.07.007
  122. Sarabi ZS, Sahebari M, Rezaie AE, Norouzi MT, Hashemzadeh K, Mirfeizi Z. Relationship between Systemic Lupus Erythematosus activity and Persistent Positive Antiphospholipid Antibodies. Curr Rheumatol Rev. 2018;14(2):145-152. https://doi.org/10.2174/1573397113666161122152553
  123. Sebastiani GD, Prevete I, Iuliano A, Minisola G. The Importance of an Early Diagnosis in Systemic Lupus Erythematosus. Isr Med Assoc J. 2016;18(3-4):212-215.
  124. Sharma SK, Rathi M, Sahoo S. Assessment of premature atherosclerosis in systemic lupus erythematosus patients with and without nephritis. Lupus. 2016;25(5):525-531. https://doi.org/10.1177/0961203315622822
  125. Shevchuk SV. Thrombocytopenia as a Marker of Cardiovascular Lesions in SLE. Bulletin of Problems of Biology and Medicine. 2014;(4):186-190 (Ukrainian)21
  126. Silva JA, Lima SC, Addobbati C et al. Association of interferon-induced helicase C domain (IFIH1) gene polymorphisms with systemic lupus erythematosus and a relevant updated meta-analysis. Genet Mol Res. 2016;15(4). https://doi.org/10.4238/gmr15048008
  127. Singh JA, Hossain A, Kotb A et al. Risk of serious infections with immunosuppressive drugs and glucocorticoids for lupus nephritis: a systematic review and network meta-analysis. BMC Med. 2016;14(1):137-140. https://doi.org/10.1186/s12916-016-0673-8
  128. Sinyachenko PO, Ignatenko GA, Dyadyk EA. Endocardium defeat and heart valves at patients with systemic lupus erythematosus (сlinico-morphological comparisons). Ukrainian morphological Almanac. 2011;14(3):149-151) (Ukrainian)
  129. Sisirak V, Ganguly D, Lewis KL, Couillault C, Tanaka L, Bolland S et al. Genetic evidence for the role of plasmacytoid dendritic cells in systemic lupus erythematosus. J Exp Med. 2014;211(10):1969-1976. https://doi.org/10.1084/jem.20132522
  130. Smrzova A, Horak P, Skacelova M et al. Intima media thickness measurement as a marker of subclinical atherosclerosis in SLE patient. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2014;158(3):404-411. https://doi.org/10.5507/bp.2013.054
  131. Solhjoo M, Bansal P, Goyal A et al. Drug-Induced Lupus Erythematosus. StatPearls Publishing, Treasure Island (FL), 2020 Jan.
  132. Soyuöz A, Karadağ Ö, Karaağaç T et al. Therapeutic plasma exchange for refractory SLE: A comparison of outcomes between different sub-phenotypes. Eur J Rheumatol. 2018;5(1):32-36. https://doi.org/10.5152/eurjrheum.2017.17088
  133. Staveri C, Karokis D, Liossis SC. New onset of lupus nephritis in two patients with SLE shortly after initiation of treatment with belimumab. Semin Arthritis Rheum. 2017;46(6):788-790. https://doi.org/10.1016/j.semarthrit.2016.09.006
  134. Steiman AJ, Urowitz MB, Ibañez D, Li TT, Gladman DD, Wither J. Anti-dsDNA and Antichromatin Antibody Isotypes in Serologically Active Clinically Quiescent Systemic Lupus Erythematosus. J Rheumatol. 2015;42(5):810-816. https://doi.org/10.3899/jrheum.140796
  135. Stojan G, Petri M. Epidemiology of systemic lupus erythematosus: an update. Curr Opin Rheumatol. 2018;30(2):144-150. https://doi.org/10.1097/BOR.0000000000000480
  136. Suárez-Fueyo A, Bradley SJ, Tsokos GC. T cells in Systemic Lupus Erythematosus. Curr Opin Immunol. 2016;43:32-38. https://doi.org/10.1016/j.coi.2016.09.001
  137. Tamaki K, Morishima S, Nakachi S. An atypical case of late-onset systemic lupus erythematosus with systemic lymphadenopathy and severe autoimmune thrombocytopenia/neutropenia mimicking malignant lymphoma. Int J Hematol. 2016;8:1-6.
  138. Tarr T, Papp G, Nagy N. Chronic high-dose glucocorticoid therapy triggers the development of chronic organ damage and worsens disease outcome in systemic lupus erythematosus. Clin Rheumatol. 2017;36:327-333. https://doi.org/10.1007/s10067-016-3492-6
  139. Tazi Z, Harmouche H, Ammouri W, Maamar M, Adnaoui M, Cacoub P. Atherosclerosis in systemic lupus erythematosus. Presse Med. 2014;43(10):1034-1047. https://doi.org/10.1016/j.lpm.2014.01.021
  140. Thomas G, Aubart FC, Chiche L et al. Lupus Myocarditis: Initial Presentation and Longterm Outcomes in a Multicentric Series of 29 Patients. J Rheumatol. 2017;44(1):24-32. https://doi.org/10.3899/jrheum.160493
  141. Touma Z, Gladman DD, Su J, Anderson N, Urowitz MB. A novel lupus activity index accounting for glucocorticoids: SLEDAI-2K glucocorticoid index. Rheumatol (Oxford, England). 2018;57(8):1370-1376. https://doi.org/10.1093/rheumatology/key103
  142. Troldborg A, Thiel S, Trendelenburg M, Friebus-Kardash J, Nehring J, Steffensen R et al. The Lectin Pathway of Complement Activation in Patients with Systemic Lupus Erythematosus. J Rheumatol. 2018;45(8):1136-1144. https://doi.org/10.3899/jrheum.171033
  143. Truszewska A, Foroncewicz B, Pączek L. The role and diagnostic value of cell-free DNA in systemic lupus erythematosus. Clin Exp Rheumatol. 2016. – Access mode : http://www.clinexprheumatol.org/abstract.aspa=10715.
  144. Tsang-A-Sjoe MW, Bultink IE, Heslinga M et al. Both prolonged remission and Lupus Low Disease Activity State are associated with reduced damage accrual in systemic lupus erythematosus. Rheumatol. (Oxford). 2017;56(1):121-128. https://doi.org/10.1093/rheumatology/kew377
  145. Tselios K, Deeb M, Gladman DD, Harvey P, Akhtari S, Mak S et al. Antimalarial-induced Cardiomyopathy in Systemic Lupus Erythematosus: As Rare as Considered? J Rheumatol. 2019;46(4):391-396. https://doi.org/10.3899/jrheum.180124
  146. Tselios K, Gladman DD, Touma Z et al. Clinical remission and low disease activity have comparable outcomes over 10 years in systemic lupus erythematosus. Arthritis Care Res. (Hoboken). 2019;71(6):822-828. https://doi.org/10.1002/acr.23720
  147. Tselios K, Gladman DD, Urowitz MB. Systemic lupus erythematosus and pulmonary arterial hypertension: links, risks, and management strategies. Open Access Rheumatol. 2017;9:1-9. https://doi.org/10.2147/OARRR.S123549
  148. Tselios K, Koumaras C, Gladman DD, Urowitz MB. Dyslipidemia in systemic lupus erythematosus: just another comorbidity? Semin Arthritis Rheum. 2016;45(5):604-610. https://doi.org/10.1016/j.semarthrit.2015.10.010
  149. Tselios K, Sheane BJ, Gladman DD, Urowitz MB. Optimal Monitoring For Coronary Heart Disease Risk in Patients with Systemic Lupus Erythematosus: A Systematic Review. J Rheumatol. 2016;43(1):54-65. https://doi.org/10.3899/jrheum.150460
  150. Tselios K, Gladman DD, Harvey P, Akhtari S, Su J, Urowitz MB. Abnormal Cardiac Biomarkers in Patients with Systemic Lupus Erythematosus and No Prior Heart Disease: A Consequence of Antimalarials? J Rheumatol. 2019;46(1):64-69. https://doi.org/10.3899/jrheum.171436
  151. Tselios K, Gladman DD, Su J, Ace O, Urowitz MB. Evolution of Risk Factors for Atherosclerotic Cardiovascular Events in Systemic Lupus Erythematosus: A Longterm Prospective Study. J Rheumatol. 2017;44(12):1841-1849. https://doi.org/10.3899/jrheum.161121
  152. Tselios K, Gladman DD, Su J, Urowitz MB. Mycophenolate Mofetil in Nonrenal Manifestations of Systemic Lupus Erythematosus: An Observational Cohort Study. J Rheumatol. 2016;43(3):552-558. https://doi.org/10.3899/jrheum.150779
  153. Tselios K, Gladman DD, Urowitz MB. How can we define low disease activity in systemic lupus erythematosus? Semin Arthritis Rheum. 2019;48(6):1035-1040. https://doi.org/10.1016/j.semarthrit.2018.10.013
  154. Tziomalos K, Gkougkourelas I, Sarantopoulos A. Arterial stiffness and peripheral arterial disease in patients with systemic lupus erythematosus. Rheumatol Int. 2017;37(2):293-298. https://doi.org/10.1007/s00296-016-3610-4
  155. Ünlü O, Zuily S, Erkan D. The clinical significance of antiphospholipid antibodies in systemic lupus erythematosus. Eur J Rheumatol. 2016;3:75-84. https://doi.org/10.5152/eurjrheum.2015.0085
  156. Urowitz MB, Su J, Gladman DD. Atherosclerotic Vascular Events in Systemic Lupus Erythematosus – an Evolving Story. J Rheumatol. 2020;47(1):66-71. https://doi.org/10.3899/jrheum.180986
  157. van Vollenhoven R, Voskuyl A, Bertsias G. A framework for remission in SLE: consensus findings from a large international task force on definitions of remission in SLE (DORIS). Ann Rheum Dis. 2017;76(3):554-561. https://doi.org/10.1136/annrheumdis-2016-209519
  158. Volkmann ER, Grossman JM, Sahakian LJ, Skaggs BJ, Gerald JF, Ragavendra N. Low physical activity is associated with proinflammatory high density lipoprotein and increased subclinical atherosclerosis in women with systemic lupus erythematosus. Apthritis Care Res. 2010;62(2):258-265. https://doi.org/10.1002/acr.20076
  159. Vukelic M, Li Y, Kyttaris VC. Novel Treatments in Lupus. Front Immunol. 2018;9:2658. https://doi.org/10.3389/fimmu.2018.02658
  160. Wang H, Cao J, Lai X. Serum Interleukin-34 Levels Are Elevated in Patients with Systemic Lupus Erythematosus. Molecules. 2017;22(35):1-8. https://doi.org/10.3390/molecules22010035
  161. Watad A, Abu Much A, Bracco D. Association between ischemic heart disease and systemic lupus erythematosus-a large case-control study. Immunol Res. 2017;64(153):1-5. https://doi.org/10.1007/s12026-016-8884-9
  162. Wu GC, Liu HR, Leng RX, Li XP, Li XM, Pan HF, Ye DQ. Subclinical atherosclerosis in patients with systemic lupus erythematosus: A systemic review and meta-analysis. Autoimmun Rev. 2016;15(1):22-37. https://doi.org/10.1016/j.autrev.2015.10.002
  163. Yaremenko OB, Petelytska LB. Systemic lupus erythematosus: clinically significant aspects. https://health-ua.com/article/5704-sistemnij-chervonij-vovchak-klnchno-znachush-aspekti). (Ukrainian)
  164. Yelnik CM, Richey M, Haiduc V. Cardiovascular Disease Prevention Counseling Program for Systemic Lupus Erythematosus Patients. Arthritis Care Res. (Hoboken). 2017;69(8):1209-1216. https://doi.org/10.1002/acr.23128
  165. Yeung KS, Chung BH, Choufani S et al. Genome-Wide DNA Methylation Analysis of Chinese Patients with Systemic Lupus Erythematosus Identified Hypomethylation in Genes Related to the Type I Interferon Pathway. PLoS One. 2017;12(1):e0169553. https://doi.org/10.1371/journal.pone.0169553
  166. Young NA, Valiente GR, Hampton JM. Estrogen-regulated STAT1 activation promotes TLR8 expression to facilitate signaling via microRNA-21 in systemic lupus erythematosus. Clin Immunol. 2016;176:12-22. https://doi.org/10.1016/j.clim.2016.12.005
  167. Yung S, Chan TM. Mechanisms of Kidney Injury in Lupus Nephritis – the Role of Anti-dsDNA Antibodies. Front Immunol. 2015;6:475. https://doi.org/10.3389/fimmu.2015.00475