Semin Thromb Hemost 2024; 50(04): 609-619
DOI: 10.1055/s-0043-1777071
Review Article

Role of Platelets in Rheumatic Chronic Autoimmune Inflammatory Diseases

Martin Jozef Péč
1   Department of Internal Medicine I, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Jakub Jurica
1   Department of Internal Medicine I, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Monika Péčová
2   Oncology Centre, Teaching Hospital Martin, Martin, Slovak Republic
3   Department of Hematology and Transfusiology, National Centre of Hemostasis and Thrombosis, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Jakub Benko
1   Department of Internal Medicine I, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
4   Department of Cardiology, Teaching Hospital Nitra, Nitra, Slovak Republic
,
Juraj Sokol
3   Department of Hematology and Transfusiology, National Centre of Hemostasis and Thrombosis, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Tomáš Bolek
1   Department of Internal Medicine I, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Marek Samec
5   Department of Medical Biology, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Tatiana Hurtová
6   Department of Dermatovenerology, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
7   Department of Infectology and Travel Medicine, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Peter Galajda
1   Department of Internal Medicine I, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
,
Matej Samoš
1   Department of Internal Medicine I, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
8   Division of Acute and Interventional Cardiology, Department of Cardiology and Angiology II, Mid-Slovakian Institute of Heart and Vessel Diseases (SÚSCCH, a.s.), Banská Bystrica, Slovak Republic
,
Marián Mokáň
1   Department of Internal Medicine I, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Martin, Slovak Republic
› Author Affiliations
Funding This study was supported by the research project of Slovak Research and Development Agency (APVV) 16-0020, by the research project of the Research Agency of Slovak Ministry of Education, Science, and Sports (VEGA) 1/0090/20, and by the research project of Comenius University (UK/318/2022).

Abstract

Platelets are essential in maintaining blood homeostasis and regulating several inflammatory processes. They constantly interact with immune cells, have immunoregulatory functions, and can affect, through immunologically active substances, endothelium, leukocytes, and other immune response components. In reverse, inflammatory and immune processes can activate platelets, which might be significant in autoimmune disease progression and arising complications. Thus, considering this interplay, targeting platelet activity may represent a new approach to treatment of autoimmune diseases. This review aims to highlight the role of platelets in the pathogenic mechanisms of the most frequent chronic autoimmune inflammatory diseases to identify gaps in current knowledge and to provide potential new targets for medical interventions.

Data Availability

All the source data are available at the corresponding author upon a reasonable request.




Publication History

Article published online:
28 November 2023

© 2023. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Lefrançais E, Ortiz-Muñoz G, Caudrillier A. et al. The lung is a site of platelet biogenesis and a reservoir for haematopoietic progenitors. Nature 2017; 544 (7648) 105-109
  • 2 Semple JW, Italiano Jr JE, Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011; 11 (04) 264-274
  • 3 van der Meijden PEJ, Heemskerk JWM. Platelet biology and functions: new concepts and clinical perspectives. Nat Rev Cardiol 2019; 16 (03) 166-179
  • 4 Brewer DB. Max Schultze (1865), G. Bizzozero (1882) and the discovery of the platelet. Br J Haematol 2006; 133 (03) 251-258
  • 5 Holinstat M. Normal platelet function. Cancer Metastasis Rev 2017; 36 (02) 195-198
  • 6 Italiano Jr JE, Battinelli EM. Selective sorting of alpha-granule proteins. J Thromb Haemost 2009; 7 Suppl 1 (Suppl. 01) 173-176
  • 7 Liu X, Gorzelanny C, Schneider SW. Platelets in skin autoimmune diseases. Front Immunol 2019; 10: 1453
  • 8 Thompson CB, Eaton KA, Princiotta SM, Rushin CA, Valeri CR. Size dependent platelet subpopulations: relationship of platelet volume to ultrastructure, enzymatic activity, and function. Br J Haematol 1982; 50 (03) 509-519
  • 9 Korniluk A, Koper-Lenkiewicz OM, Kamińska J, Kemona H, Dymicka-Piekarska V. Mean platelet volume (MPV): new perspectives for an old marker in the course and prognosis of inflammatory conditions. Mediators Inflamm 2019; 2019: 9213074
  • 10 Li B, Zhou P, Liu Y. et al. Platelet-to-lymphocyte ratio in advanced cancer: review and meta-analysis. Clin Chim Acta 2018; 483: 48-56
  • 11 Luo Z, Zhang W, Chen L, Xu N. Prognostic value of neutrophil:lymphocyte and platelet:lymphocyte ratios for 28-day mortality of patients with AECOPD. Int J Gen Med 2021; 14: 2839-2848
  • 12 Wang H, Li L, Ma Y. Platelet-to-lymphocyte ratio a potential prognosticator in acute myocardial infarction: a prospective longitudinal study. Clin Cardiol 2023; 46 (06) 632-638
  • 13 André P. P-selectin in haemostasis. Br J Haematol 2004; 126 (03) 298-306
  • 14 Gasparyan AY, Ayvazyan L, Mukanova U, Yessirkepov M, Kitas GD. The platelet-to-lymphocyte ratio as an inflammatory marker in rheumatic diseases. Ann Lab Med 2019; 39 (04) 345-357
  • 15 Gieger C, Radhakrishnan A, Cvejic A. et al. New gene functions in megakaryopoiesis and platelet formation. Nature 2011; 480 (7376) 201-208
  • 16 Bahou WF, Gnatenko DV. Platelet transcriptome: the application of microarray analysis to platelets. Semin Thromb Hemost 2004; 30 (04) 473-484
  • 17 Clancy L, Freedman JE. The role of circulating platelet transcripts. J Thromb Haemost 2015; 13 (Suppl. 01) S33-S39
  • 18 Lindsay CR, Edelstein LC. MicroRNAs in platelet physiology and function. Semin Thromb Hemost 2016; 42 (03) 215-222
  • 19 Thibord F, Klarin D, Brody JA. et al; Global Biobank Meta-Analysis Initiative; Estonian Biobank Research Team; 23andMe Research Team; Biobank Japan; CHARGE Hemostasis Working Group. Cross-ancestry investigation of venous thromboembolism genomic predictors. Circulation 2022; 146 (16) 1225-1242
  • 20 Kachuri L, Jeon S, DeWan AT. et al. Genetic determinants of blood-cell traits influence susceptibility to childhood acute lymphoblastic leukemia. Am J Hum Genet 2021; 108 (10) 1823-1835
  • 21 Fisher MH, Di Paola J. Genomics and transcriptomics of megakaryocytes and platelets: implications for health and disease. Res Pract Thromb Haemost 2018; 2 (04) 630-639
  • 22 Ghouse J, Tragante V, Ahlberg G. et al. Genome-wide meta-analysis identifies 93 risk loci and enables risk prediction equivalent to monogenic forms of venous thromboembolism. Nat Genet 2023; 55 (03) 399-409
  • 23 Michalek IM, Loring B, John SM. A systematic review of worldwide epidemiology of psoriasis. J Eur Acad Dermatol Venereol 2017; 31 (02) 205-212
  • 24 Vaengebjerg S, Skov L, Egeberg A, Loft ND. Prevalence, incidence, and risk of cancer in patients with psoriasis and psoriatic arthritis: a systematic review and meta-analysis. JAMA Dermatol 2020; 156 (04) 421-429
  • 25 Garshick MS, Ward NL, Krueger JG, Berger JS. Cardiovascular risk in patients with psoriasis: JACC review topic of the week. J Am Coll Cardiol 2021; 77 (13) 1670-1680
  • 26 Snekvik I, Nilsen TIL, Romundstad PR, Saunes M. Psoriasis and cardiovascular disease risk factors: the HUNT study, Norway. J Eur Acad Dermatol Venereol 2018; 32 (05) 776-782
  • 27 Fan Z, Wang L, Jiang H, Lin Y, Wang Z. Platelet dysfunction and its role in the pathogenesis of psoriasis. Dermatology 2021; 237 (01) 56-65
  • 28 Kragballe K, Fallon JD. Increased aggregation and arachidonic acid transformation by psoriatic platelets: evidence that platelet-derived 12-hydroxy-eicosatetraenoic acid increases keratinocyte DNA synthesis in vitro. Arch Dermatol Res 1986; 278 (06) 449-453
  • 29 Kasperska-Zajac A, Brzoza Z, Rogala B. Platelet function in cutaneous diseases. Platelets 2008; 19 (05) 317-321 [published correction appears in Platelets. 2009 Feb;20(1):74]
  • 30 Vila L, Cullaré C, Solá J, Puig L, de Castellarnau C, de Moragas JM. Cyclooxygenase activity is increased in platelets from psoriatic patients. J Invest Dermatol 1991; 97 (05) 922-926
  • 31 Garshick MS, Tawil M, Barrett TJ. et al. Activated platelets induce endothelial cell inflammatory response in psoriasis via COX-1. Arterioscler Thromb Vasc Biol 2020; 40 (05) 1340-1351
  • 32 Tamagawa-Mineoka R, Katoh N, Kishimoto S. Platelet activation in patients with psoriasis: increased plasma levels of platelet-derived microparticles and soluble P-selectin. J Am Acad Dermatol 2010; 62 (04) 621-626
  • 33 Chandrashekar L, Rajappa M, Revathy G. et al. Is enhanced platelet activation the missing link leading to increased cardiovascular risk in psoriasis?. Clin Chim Acta 2015; 446: 181-185
  • 34 Pelletier F, Garnache-Ottou F, Biichlé S. et al. Effects of anti-TNF-α agents on circulating endothelial-derived and platelet-derived microparticles in psoriasis. Exp Dermatol 2014; 23 (12) 924-925
  • 35 Merten M, Pakala R, Thiagarajan P, Benedict CR. Platelet microparticles promote platelet interaction with subendothelial matrix in a glycoprotein IIb/IIIa-dependent mechanism. Circulation 1999; 99 (19) 2577-2582
  • 36 Farag AG, Zytoon AA, Habib MS. et al. Mean platelet volume: an immanent predictor of subclinical atherosclerosis in psoriatic patients compared with interleukin-1α and interleukin-6. J Egypt Womens Dermatol Soc 2018; 15 (02) 80-87
  • 37 Mahrous EM. The relationship between platelet volume and risk of atherosclerosis in patients with psoriasis. Egypt J Dermatol Venerol 2018; 38 (01) 29
  • 38 Raghavan V, Radha RKN, Rao RK, Kuberan A. A correlative study between platelet count, mean platelet volume and red cell distribution width with the disease severity index in psoriasis patients. J Clin Diagn Res 2017; 11 (09) EC13-EC16
  • 39 Saleh HM, Attia EA, Onsy AM, Saad AA, Abd Ellah MM. Platelet activation: a link between psoriasis per se and subclinical atherosclerosis–a case-control study. Br J Dermatol 2013; 169 (01) 68-75
  • 40 Garbaraviciene J, Diehl S, Varwig D. et al. Platelet P-selectin reflects a state of cutaneous inflammation: possible application to monitor treatment efficacy in psoriasis. Exp Dermatol 2010; 19 (08) 736-741
  • 41 Nageen S, Shah R, Sharif S, Jamgochian M, Waqas N, Rao B. Platelet count, mean platelet volume, and red cell distribution width as markers for psoriasis severity. J Drugs Dermatol 2022; 21 (02) 156-161
  • 42 Hammad R, Hamdino M, El-Nasser AM. Role of neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio, mean platelet volume in egyptian patients with psoriasis vulgaris. Egypt J Immunol 2020; 27 (01) 157-168
  • 43 Özkur E, Şeremet S, Afşar FŞ, Altunay İK, Çalıkoğlu EE. Platelet count and mean platelet volume in psoriasis patients. Sisli Etfal Hastan Tip Bul 2018; 54 (01) 58-61
  • 44 Kılıç S, Reşorlu H, Işik S. et al. Association between mean platelet volume and disease severity in patients with psoriasis and psoriatic arthritis. Postepy Dermatol Alergol 2017; 34 (02) 126-130
  • 45 Kwiek B, Narbutt J, Sysa-Jędrzejowska A, Langner A, Lesiak A. Long-term treatment of chronic plaque psoriasis with biological drugs can control platelet activation: targeting the bridge between inflammation and atherothrombosis. Postepy Dermatol Alergol 2017; 34 (02) 131-137
  • 46 Unal M. Platelet mass index is increased in psoriasis. A possible link between psoriasis and atherosclerosis. Arch Med Sci Atheroscler Dis 2016; 1 (01) e145-e149
  • 47 Işik S, Kılıç S, Öğretmen Z. et al. The correlation between the psoriasis area severity index and ischemia-modified albumin, mean platelet volume levels in patients with psoriasis. Postepy Dermatol Alergol 2016; 33 (04) 290-293
  • 48 Kim DS, Lee J, Kim SH, Kim SM, Lee MG. Mean platelet volume is elevated in patients with psoriasis vulgaris. Yonsei Med J 2015; 56 (03) 712-718
  • 49 Canpolat F, Akpinar H, Eskioğlu F. Mean platelet volume in psoriasis and psoriatic arthritis. Clin Rheumatol 2010; 29 (03) 325-328
  • 50 Ataseven A, Ataseven H, Ozturk P, Ozdemir M, Kesli R. Levels of serum soluble p-selectin and e-selectin in psoriatıc patients. Ann Dermatol 2014; 26 (02) 275-277
  • 51 Borská L, Fiala Z, Krejsek J. et al. Selected immunological changes in patients with Goeckerman's therapy TNF-alpha, sE-selectin, sP-selectin, sICAM-1 and IL-8. Physiol Res 2006; 55 (06) 699-706
  • 52 Li L, Yu J, Zhou Z. Platelet-associated parameters in patients with psoriasis: a PRISMA-compliant systematic review and meta-analysis. Medicine (Baltimore) 2021; 100 (50) e28234
  • 53 Yi P, Jiang J, Wang Z. et al. Comparison of mean platelet volume (MPV) and red blood cell distribution width (RDW) between psoriasis patients and controls: a systematic review and meta-analysis. PLoS One 2022; 17 (02) e0264504
  • 54 Liu Z, Perry LA, Morgan V. The association between platelet indices and presence and severity of psoriasis: a systematic review and meta-analysis. Clin Exp Med 2023; 23 (02) 333-346
  • 55 Pourani MR, Abdollahimajd F, Zargari O, Shahidi Dadras M. Soluble biomarkers for diagnosis, monitoring, and therapeutic response assessment in psoriasis. J Dermatolog Treat 2022; 33 (04) 1967-1974
  • 56 Armstrong AW, Harskamp CT, Armstrong EJ. The association between psoriasis and obesity: a systematic review and meta-analysis of observational studies. Nutr Diabetes 2012; 2 (12) e54
  • 57 Purdy JC, Shatzel JJ. The hematologic consequences of obesity. Eur J Haematol 2021; 106 (03) 306-319
  • 58 Raoux L, Moszkowicz D, Vychnevskaia K. et al. Effect of bariatric surgery-induced weight loss on platelet count and mean platelet volume: a 12-month follow-up study. Obes Surg 2017; 27 (02) 387-393
  • 59 Chiang TM, Takayama H, Postlethwaite AE. Increase in platelet non-integrin type I collagen receptor in patients with systemic sclerosis. Thromb Res 2006; 117 (03) 299-306
  • 60 Dees C, Akhmetshina A, Zerr P. et al. Platelet-derived serotonin links vascular disease and tissue fibrosis. J Exp Med 2011; 208 (05) 961-972
  • 61 Biondi ML, Marasini B, Bianchi E, Agostoni A. Plasma free and intraplatelet serotonin in patients with Raynaud's phenomenon. Int J Cardiol 1988; 19 (03) 335-339
  • 62 Chaturvedi S, Misra DP, Prasad N. et al. 5-HT2 and 5-HT2B antagonists attenuate pro-fibrotic phenotype in human adult dermal fibroblasts by blocking TGF-β1 induced non-canonical signaling pathways including STAT3 : implications for fibrotic diseases like scleroderma. Int J Rheum Dis 2018; 21 (12) 2128-2138
  • 63 Atamas SP, White B. Cytokine regulation of pulmonary fibrosis in scleroderma. Cytokine Growth Factor Rev 2003; 14 (06) 537-550
  • 64 Truchetet ME, Demoures B, Eduardo Guimaraes J. et al; Fédération Hospitalo-Universitaire ACRONIM. Platelets induce thymic stromal lymphopoietin production by endothelial cells: contribution to fibrosis in human systemic sclerosis. Arthritis Rheumatol 2016; 68 (11) 2784-2794
  • 65 Mandel J, Casari M, Stepanyan M, Martyanov A, Deppermann C. Beyond hemostasis: platelet innate immune interactions and thromboinflammation. Int J Mol Sci 2022; 23 (07) 3868
  • 66 Koupenova M, Clancy L, Corkrey HA, Freedman JE. Circulating platelets as mediators of immunity, inflammation, and thrombosis. Circ Res 2018; 122 (02) 337-351
  • 67 Mabrouk M, Guessous F, Naya A, Merhi Y, Zaid Y. The pathophysiological role of platelet-derived extracellular vesicles. Semin Thromb Hemost 2023; 49 (03) 279-283
  • 68 Bergmann CB, Hefele F, Unger M. et al. Platelets modulate the immune response following trauma by interaction with CD4+ T regulatory cells in a mouse model. Immunol Res 2016; 64 (02) 508-517
  • 69 Prescott RJ, Freemont AJ, Jones CJ, Hoyland J, Fielding P. Sequential dermal microvascular and perivascular changes in the development of scleroderma. J Pathol 1992; 166 (03) 255-263
  • 70 Yayla ME, İlgen U, Okatan İE. et al. Association of simple hematological parameters with disease manifestations, activity, and severity in patients with systemic sclerosis. Clin Rheumatol 2020; 39 (01) 77-83
  • 71 Yolbas S, Yildirim A, Gozel N, Uz B, Koca SS. Hematological indices may be useful in the diagnosis of systemic lupus erythematosus and in determining disease activity in Behçet's disease. Med Princ Pract 2016; 25 (06) 510-516
  • 72 Soydinc S, Turkbeyler IH, Pehlivan Y. et al. Mean platelet volume seems to be a valuable marker in patients with systemic sclerosis. Inflammation 2014; 37 (01) 100-106
  • 73 Yalçınkaya Y, Adın-Çınar S, Artim-Esen B. et al. Capillaroscopic findings and vascular biomarkers in systemic sclerosis: association of low CD40L levels with late scleroderma pattern. Microvasc Res 2016; 108: 17-21
  • 74 Yalçinkaya Y, Çinar S, Artim-Esen B. et al. The relationship between vascular biomarkers and disease characteristics in systemic sclerosis: elevated MCP-1 is predominantly associated with fibrotic manifestations. Clin Exp Rheumatol 2016; 34 (5, Suppl 100): 110-114
  • 75 Iversen LV, Østergaard O, Ullman S. et al. Circulating microparticles and plasma levels of soluble E- and P-selectins in patients with systemic sclerosis. Scand J Rheumatol 2013; 42 (06) 473-482
  • 76 Olewicz-Gawlik A, Danczak-Pazdrowska A, Klama K. et al. Blood serum levels of amino-terminal pro-C-type natriuretic peptide in patients with systemic sclerosis. Connect Tissue Res 2010; 51 (02) 83-87
  • 77 Ateş A, Kinikli G, Turgay M, Duman M. Serum-soluble selectin levels in patients with rheumatoid arthritis and systemic sclerosis. Scand J Immunol 2004; 59 (03) 315-320
  • 78 Taha SI, Samaan SF, Ibrahim RA, Moustafa NM, El-Sehsah EM, Youssef MK. Can complete blood count picture tell us more about the activity of rheumatological diseases?. Clin Med Insights Arthritis Musculoskelet Disord 2022; 15: 117 95441221089182
  • 79 Talat M, An Allah M, Khalifa NA, Sakr MMH, Mohammed EM. K Amin E, Mean platelet volume in children with systemic lupus erythematosus. Lupus 2021; 30 (01) 103-108
  • 80 Wirestam L, Gullstrand B, Jern A. et al. Low intra-individual variation in mean platelet volume over time in systemic lupus erythematosus. Front Med (Lausanne) 2021; 8: 638750
  • 81 Hartmann LT, Alegretti AP, Machado ABMP. et al. Assessment of mean platelet volume in patients with systemic lupus erythematosus. Open Rheumatol J 2018; 12: 129-138
  • 82 Qin B, Ma N, Tang Q. et al. Neutrophil to lymphocyte ratio (NLR) and platelet to lymphocyte ratio (PLR) were useful markers in assessment of inflammatory response and disease activity in SLE patients. Mod Rheumatol 2016; 26 (03) 372-376
  • 83 Delgado-García G, Galarza-Delgado DÁ, Colunga-Pedraza I. et al. Mean platelet volume is decreased in adults with active lupus disease. Rev Bras Reumatol Engl Ed 2016; 56 (06) 504-508
  • 84 Yavuz S, Ece A. Mean platelet volume as an indicator of disease activity in juvenile SLE. Clin Rheumatol 2014; 33 (05) 637-641
  • 85 Safak S, Uslu AU, Serdal K, Turker T, Soner S, Lutfi A. Association between mean platelet volume levels and inflammation in SLE patients presented with arthritis. Afr Health Sci 2014; 14 (04) 919-924
  • 86 Cieślik P, Hrycek A. Pentraxin 3 as a biomarker of local inflammatory response to vascular injury in systemic lupus erythematosus. Autoimmunity 2015; 48 (04) 242-250
  • 87 Lood C, Tydén H, Gullstrand B. et al. Platelet-derived S100A8/A9 and cardiovascular disease in systemic lupus erythematosus. Arthritis Rheumatol 2016; 68 (08) 1970-1980
  • 88 Ma CY, Jiao YL, Zhang J. et al. Elevated plasma level of HMGB1 is associated with disease activity and combined alterations with IFN-α and TNF-α in systemic lupus erythematosus. Rheumatol Int 2012; 32 (02) 395-402
  • 89 Linge P, Fortin PR, Lood C, Bengtsson AA, Boilard E. The non-haemostatic role of platelets in systemic lupus erythematosus. Nat Rev Rheumatol 2018; 14 (04) 195-213
  • 90 Lood C, Tydén H, Gullstrand B. et al. Platelet activation and anti-phospholipid antibodies collaborate in the activation of the complement system on platelets in systemic lupus erythematosus. PLoS One 2014; 9 (06) e99386
  • 91 Nagahama M, Nomura S, Ozaki Y, Yoshimura C, Kagawa H, Fukuhara S. Platelet activation markers and soluble adhesion molecules in patients with systemic lupus erythematosus. Autoimmunity 2001; 33 (02) 85-94
  • 92 Takeda I, Kaise S, Nishimaki T, Kasukawa R. Soluble P-selectin in the plasma of patients with connective tissue diseases. Int Arch Allergy Immunol 1994; 105 (02) 128-134
  • 93 Uzkeser H, Keskin H, Haliloglu S. et al. Is mean platelet volume related to disease activity in systemic lupus erythematosus?. Int J Clin Pract 2021; 75 (11) e14676
  • 94 Chen SY, Du J, Lu XN, Xu JH. Platelet distribution width as a novel indicator of disease activity in systemic lupus erythematosus. J Res Med Sci 2018; 23: 48
  • 95 Baldwin III WM, Kuo HH, Morrell CN. Platelets: versatile modifiers of innate and adaptive immune responses to transplants. Curr Opin Organ Transplant 2011; 16 (01) 41-46
  • 96 Koupenova M, Livada AC, Morrell CN. Platelet and megakaryocyte roles in innate and adaptive immunity. Circ Res 2022; 130 (02) 288-308
  • 97 Bai M, Xing L, Feng J, Cui C, Huang L, Liang G. Mean platelet volume could reflect disease activity of adult patients with systemic lupus erythematosus. Clin Lab 2016; 62 (07) 1317-1322
  • 98 Ma L, Zeng A, Chen B, Chen Y, Zhou R. Neutrophil to lymphocyte ratio and platelet to lymphocyte ratio in patients with systemic lupus erythematosus and their correlation with activity: a meta-analysis. Int Immunopharmacol 2019; 76: 105949
  • 99 Lee JL, Sinnathurai P, Buchbinder R, Hill C, Lassere M, March L. Biologics and cardiovascular events in inflammatory arthritis: a prospective national cohort study. Arthritis Res Ther 2018; 20 (01) 171
  • 100 Larsson I. Patients' conceptions of their own influence on good treatment response to biological therapy in chronic inflammatory arthritis. Patient Prefer Adherence 2017; 11: 1057-1067
  • 101 van Riel PL, Renskers L. The Disease Activity Score (DAS) and the Disease Activity Score using 28 joint counts (DAS28) in the management of rheumatoid arthritis. Clin Exp Rheumatol 2016; 34 (5, Suppl 101): S40-S44
  • 102 Gossec L, Portier A, Landewé R. et al. Preliminary definitions of ‘flare’ in axial spondyloarthritis, based on pain, BASDAI and ASDAS-CRP: an ASAS initiative. Ann Rheum Dis 2016; 75 (06) 991-996
  • 103 Michelsen B, Sexton J, Smolen JS. et al. Can disease activity in patients with psoriatic arthritis be adequately assessed by a modified Disease Activity index for PSoriatic Arthritis (DAPSA) based on 28 joints?. Ann Rheum Dis 2018; 77 (12) 1736-1741
  • 104 Duffield SJ, Miller N, Zhao S, Goodson NJ. Concomitant fibromyalgia complicating chronic inflammatory arthritis: a systematic review and meta-analysis. Rheumatology (Oxford) 2018; 57 (08) 1453-1460
  • 105 Ponomarev ED. Fresh evidence for platelets as neuronal and innate immune cells: their role in the activation, differentiation, and deactivation of Th1, Th17, and Tregs during tissue inflammation. Front Immunol 2018; 9: 406
  • 106 Boilard E, Blanco P, Nigrovic PA. Platelets: active players in the pathogenesis of arthritis and SLE. Nat Rev Rheumatol 2012; 8 (09) 534-542
  • 107 Zhou Z, Chen H, Ju H, Sun M, Jin H. Platelet indices in patients with chronic inflammatory arthritis: a systematic review and meta-analysis. Platelets 2020; 31 (07) 834-844
  • 108 Deng J, Xu S, Gao X, Xu S, Shuai Z, Pan F. Red cell distribution width and mean platelet volume in patients with ankylosing spondylitis: a systematic review and meta-analysis. J Clin Rheumatol 2021; 27 (07) 292-297
  • 109 Song GG, Lee YH. Red cell distribution width, platelet-to-lymphocyte ratio, and mean platelet volume in ankylosing spondylitis and their correlations with inflammation: a meta-analysis. Mod Rheumatol 2020; 30 (05) 894-899
  • 110 Kamanli A, Naziroğlu M, Aydilek N, Hacievliyagil C. Plasma lipid peroxidation and antioxidant levels in patients with rheumatoid arthritis. Cell Biochem Funct 2004; 22 (01) 53-57
  • 111 Kisacik B, Tufan A, Kalyoncu U. et al. Mean platelet volume (MPV) as an inflammatory marker in ankylosing spondylitis and rheumatoid arthritis. Joint Bone Spine 2008; 75 (03) 291-294
  • 112 Gasparyan AY, Stavropoulos-Kalinoglou A, Toms TE, Douglas KM, Kitas GD. Association of mean platelet volume with hypertension in rheumatoid arthritis. Inflamm Allergy Drug Targets 2010; 9 (01) 45-50
  • 113 Ustun N, Ulasli AM, Ustun I, Yula E, Yagiz AE, Guler H. Mean platelet volume level in patients with ankylosing spondylitis and its relationship with disease activity and presence of cardiovascular risk factors. Eur J Gen Med 2014; 11 (04) 239-243
  • 114 Kim DS, Shin D, Lee MS. et al. Assessments of neutrophil to lymphocyte ratio and platelet to lymphocyte ratio in Korean patients with psoriasis vulgaris and psoriatic arthritis. J Dermatol 2016; 43 (03) 305-310
  • 115 Huang Y, Deng W, Zheng S. et al. Relationship between monocytes to lymphocytes ratio and axial spondyloarthritis. Int Immunopharmacol 2018; 57: 43-46
  • 116 Gudowska M, Gruszewska E, Wrona A. et al. The profile of serum transferrin isoforms in rheumatoid arthritis. J Clin Rheumatol 2019; 25 (04) 159-162
  • 117 Nakarai A, Kato J, Hiraoka S. et al. Slight increases in the disease activity index and platelet count imply the presence of active intestinal lesions in C-reactive protein-negative Crohn's disease patients. Intern Med 2014; 53 (17) 1905-1911
  • 118 Vona R, Di Franco M, Gambardella L. et al. Potential role of platelets for atherosclerotic events in rheumatoid arthritis. FEBS Open Bio 2018; 8 (12) 1888
  • 119 Kozaci LD, Sari I, Alacacioglu A, Akar S, Akkoc N. Evaluation of inflammation and oxidative stress in ankylosing spondylitis: a role for macrophage migration inhibitory factor. Mod Rheumatol 2010; 20 (01) 34-39
  • 120 Deyab G, Hokstad I, Whist JE. et al. Methotrexate and anti-tumor necrosis factor treatment improves endothelial function in patients with inflammatory arthritis. Arthritis Res Ther 2017; 19 (01) 232
  • 121 Shimizu Y, Sato S, Koyamatsu J. et al. Platelets as an indicator of vascular repair in elderly Japanese men. Oncotarget 2016; 7 (29) 44919-44926
  • 122 Jeong Y, Kim JW, You HJ. et al. Gut microbial composition and function are altered in patients with early rheumatoid arthritis. J Clin Med 2019; 8 (05) 693
  • 123 Wen C, Zheng Z, Shao T. et al. Quantitative metagenomics reveals unique gut microbiome biomarkers in ankylosing spondylitis. [published correction appears in Genome Biol. 2017 Nov 8;18(1):214] Genome Biol 2017; 18 (01) 142
  • 124 Yoon HY, Kim HN, Lee SH. et al. The relationship between platelet count and host gut microbiota: a population-based retrospective cross-sectional study. J Clin Med 2019; 8 (02) 230
  • 125 Ed Rainger G, Chimen M, Harrison MJ. et al. The role of platelets in the recruitment of leukocytes during vascular disease. Platelets 2015; 26 (06) 507-520
  • 126 Eren Karanis Mİ, Küçükosmanoğlu İ, Oltulu P, Kılınç F, Özer İ. Relationship between histomorphological findings and platelet activation in psoriasis. J Cosmet Dermatol 2022; 21 (11) 6129-6133
  • 127 Garshick MS, Rosenthal PB, Luttrell-Williams E, Cronstein BN, Berger JS. Ticagrelor added to methotrexate improves rheumatoid arthritis disease severity. Rheumatology (Oxford) 2021; 60 (11) 5473-5475
  • 128 Korkmaz S. Mean platelet volume and platelet distribution width levels in patients with mild psoriasis vulgaris with metabolic syndrome. Postepy Dermatol Alergol 2018; 35 (04) 367-371
  • 129 Khan A, Haider I, Ayub M, Khan S. Mean platelet volume (MPV) as an indicator of disease activity and severity in lupus. F1000 Res 2017; 6: 126
  • 130 Frijns CJ, Derksen RH, De Groot PG, Algra A, Fijnheer R. Lupus anticoagulant and history of thrombosis are not associated with persistent endothelial cell activation in systemic lupus erythematosus. Clin Exp Immunol 2001; 125 (01) 149-154