Composition of pericardial fluid (PF) may reveal immunological processes influencing oxidative stress and microcirculation of different tissues of the heart and may play a role in the course of myocardial infarction, atherosclerosis, and aortic stenosis.
PATIENTS AND METHODS:
We investigated lymphocyte populations, cardiovascular markers and immunoglobulin composition in PF and blood samples of patients undergoing CABG operation and compared them to those who had aortic valve surgery.
RESULTS:
The amount of CD8 + T, NK, memoT and activated T-cytotoxic cells were elevated in PF compared to blood, but naiveT and activated T-helper cell ratio were lower in PF. Amount of activated T-helper cells and regulatory T-lymphocytes were elevated in CABG participants in both PF and blood. INKT cells represented the only regulatory lymphocyte population reaching significantly higher concentration in PF than in blood. IL-6 and MCP1 level were elevated in PF compared to blood and MCP1 plasma level was markedly elevated in CABG group.
CONCLUSIONS:
Our study describes a comprehensive immunological analysis of PF in humans for the first time. We showed that the investigated lymphocyte populations and cardiovascular markers in PF have significantly different distribution compared to blood, and lymphocyte populations show different compartmentization in coronary disease and aortic stenosis.
SipahiI. Bypass grafting versus percutaneous intervention in multivessel coronary disease: The current state. Curr Cardiol Rep. 2015;17(2):7.
2.
GaughanJ, KobelC. Coronary artery bypass grafts and diagnosis related groups: Patient classification and hospital reimbursement in 10 European countries. Health Econ Rev. 2014;4(1):4.
3.
LindroosM, KupariM, HeikkiläJ, TilvisR. Prevalence of aortic valve abnormalities in the elderly: An echocardiographic study of a random population sample. J Am Coll Cardiol. 1993;21(5):1220–5.
4.
González-HerreraL, ValenzuelaA, RamosV, BlázquezA, VillanuevaE. Cardiac troponin T determination by a highly sensitive assay in postmortem serum and pericardial fluid. Forensic Sci Med Pathol. 2016; doi: 10.1007/s12024-016-9749-1
5.
MebazaaA, WetzelRC, Dodd-OJM, RedmondEM, ShahAM, MaedaK, MaistreG, LakattaEG, RobothamJL. Potential paracrine role of the pericardium in the regulation of cardiac function. Cardiovasc Res. 1998;40(2):332–42.
6.
Ben-HorinS, ShinfeldA, KachelE, ChetritA, LivnehA. The composition of normal pericardial fluid and its implications for diagnosing pericardial effusions. Am J Med. 2005;118(6):636–40.
7.
Ben-HorinS, BankI, ShinfeldA, KachelE, GuettaV, LivnehA. Diagnostic Value of the Biochemical Composition of Pericardial Effusions in Patients Undergoing Pericardiocentesis. Am J Cardiol. 2007;99(9):1294–7.
8.
RiemannD, WollertHG, MenschikowskiJ, MittenzweiS, LangnerJ. Immunophenotype of lymphocytes in pericardial fluid from patients with different forms of heart disease. Int Arch Allergy Immunol. 1994;104(1):48–56.
9.
VogiatzidisK, ZarogiannisSG, AidonidisI, SolenovEI, MolyvdasP-A, GourgoulianisKI, HatzoglouC. Physiology of pericardial fluid production and drainage. Front Physiol. 2015;6:62.
10.
CoatsAJ. Pericardial fluid - Dispensable or indispensable fluid and an example of patentable bio-diversity. Int J Cardiol. 2001;77(2-3):109–11.
11.
HofmannU, BeyersdorfN, WeiratherJ, PodolskayaA, BauersachsJ, ErtlG, KerkauT, FrantzS. Activation of CD4+T lymphocytes improves wound healing and survival after experimental myocardial infarction in mice. Circulation. 2012;125(13):1652–63.
12.
FoksAC, LichtmanAH, KuiperJ. Treating atherosclerosis with regulatory T cells. Arterioscler Thromb Vasc Biol. 2015;35(2):280–7.
LiuL-L, LuJ-L, ChaoP-L, LinL-R, ZhangZ-Y, YangT-C. Lower prevalence of circulating invariant natural killer T (iNKT) cells in patients with acute myocardial infarction undergoing primary coronary stenting. Int Immunopharmacol. 2011;11(4):480–4.
15.
AnaneLH, EdwardsKM, BurnsVE, DraysonMT, RiddellNE, van ZantenJJCSV, WallaceGR, MillsPJ, BoschJA. Mobilization of gammadelta T lymphocytes in response to psychological stress, exercise, and beta-agonist infusion. Brain Behav Immun. 2009;23(6):823–9.
NapoleãoP, SelasM, FreixoC, CarmoMM, Viegas-CrespoAM, FerreiraRC, PinheiroT. T lymphocytes alterations are associated with oxidized LDL, troponin T, white blood cells and C-reactive protein during acute myocardial infarction. Clin Hemorheol Microcirc. 2013;55(3):349–58.
18.
MathieuP, BoucharebR, BoulangerMC. Innate and Adaptive Immunity in Calcific Aortic Valve Disease. J Immunol Res. 2015;2015:851945.
19.
WinchesterR, WiesendangerM, O’BrienW, ZhangH-Z, MaurerMS, GillamLD, SchwartzA, MarboeC, StewartAS. Circulating activated and effector memory T cells are associated with calcification and clonal expansions in bicuspid and tricuspid valves of calcific aortic stenosis. J Immunol. 2011;187(2):1006–14.
20.
WuHD, MaurerMS, FriedmanRA, MarboeCC, Ruiz-VazquezEM, RamakrishnanR, SchwartzA, TilsonMD, StewartAS, WinchesterR. The lymphocytic infiltration in calcific aortic stenosis predominantly consists of clonally expanded T cells. J Immunol. 2007;178(8):5329–39.
Gibson aT, SegalMB. A study of the composition of pericardial fluid, with special reference to the probable mechanism of fluid formation. J Physiol. 1978;277:367–77.
23.
GwechenbergerM, MendozaLH, YoukerKA, FrangogiannisNG, SmithCW, MichaelLH, EntmanML. Cardiac myocytes produce interleukin-6 in culture and in viable border zone of reperfused infarctions. Circulation. 1999;99(4):546–51.
ZhangW, WangJ, ShuY, et al. Impaired thymic export and increased apoptosis account for regulatory T cell defects in patients with non-ST segment elevation acute coronary syndrome. J Biol Chem. 2012;287(41):34157–66.
27.
HanS, LiuP, ZhangW, et al. The opposite-direction modulation of CD4+CD25+Tregs and T helper 1 cells in acute coronary syndromes. Clin Immunol. 2007;124(1):90–7.
28.
GetzGS, ReardonCA. Natural killer T cells in atherosclerosis. Nat Rev Cardiol. 2017; doi: 10.1038/nrcardio.2017.2
29.
JamesonSC, LeeYJ, HogquistKA. Innate memory T cells. Adv Immunol. 2015;126:173–213.
30.
TsiantoulasD, SageAP, MallatZ, BinderCJ. Targeting B cells in atherosclerosis: Closing the gap from bench to bedside. Arterioscler Thromb Vasc Biol. 2015;35(2):296–302.
31.
ZouggariY, Ait-OufellaH, BonninP, et al. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat Med. 2013;19(10):1273–80.
32.
AtkinsonC, QiaoF, YangX, ZhuP, ReavesN, KulikL, GoddardM, HolersVM, TomlinsonS. Targeting pathogenic postischemic self-recognition by natural IgM to protect against posttransplantation cardiac reperfusion injury. Circulation. 2015;131(13):1171–80.
33.
LimanaF, BertolamiC, MangoniA, et al. Myocardial infarction induces embryonic reprogramming of epicardial c-kit+cells: Role of the pericardial fluid. J Mol Cell Cardiol. 2010;48(4):609–18.
34.
ShibasakiI, NishikimiT, MochizukiY, et al. Greater expression of inflammatory cytokines, adrenomedullin, and natriuretic peptide receptor-C in epicardial adipose tissue in coronary artery disease. Regul Pept. 2010;165(2-3):210–7.
35.
YuH, ZengY, HuJ, LiC. Fluid shear stress induces the secretion of monocyte chemoattractant protein-1 in cultured human umbilical vein endothelial cells. Clin Hemorheol Microcirc. 2002;26(3):199–207.
36.
UrschelK, CichaI, DanielWG, GarlichsCD. Shear stress patterns affect the secreted chemokine profile in endothelial cells. Clin Hemorheol Microcirc. 2012;50(1-2):143–52.
37.
MenetE, CorbiP, AnceyC, MorelF, DelwailA, GarciaM, OstaA-MM, WijdenesJ, PotreauD, LecronJ-CC. Interleukine-6 (IL-6) synthesis and gp130 expression by human pericardium. Eur Cytokine Netw. 2002;12(4):639–46.
38.
FongSW, FewLL, See TooWC, KhooBY, Nik IbrahimNNI, YahayaSA, YusofZ, Mohd AliR, Abdul RahmanAR, Yvonne-TeeGB. Systemic and coronary levels of CRP, MPO, sCD40L and PlGF in patients with coronary artery disease. BMC Res Notes. 2015;8:679.
39.
GuoL, SunG, WangG, NingW, ZhaoK. Soluble P-selectin promotes acute myocardial infarction onset but not severity. Mol Med Rep. 2015;11:2027–33.
40.
BielinskiSJ, et al. P-selectin and subclinical and clinical atherosclerosis: The Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis. 2015;240:3–9.
41.
LimanaF, ZacheoA, MociniD, et al. Identification of myocardial and vascular precursor cells in human and mouse epicardium. Circ Res. 2007;101(12):1255–65.
42.
BlázquezR, Sánchez-MargalloFM, CrisóstomoV, BáezC, MaestreJ, ÁlvarezV, CasadoJG. Intrapericardial Delivery of Cardiosphere-Derived Cells: An Immunological Study in a Clinically Relevant Large Animal Model. PloSOne. 2016;11(2):e0149001.
