692
Views
50
CrossRef citations to date
0
Altmetric
Review

The pathophysiology of thrombocytopenia in chronic liver disease

, , &
Pages 39-50 | Published online: 15 Apr 2016

References

  • QamarAAGraceNDGroszmannRJIncidence, prevalence, and clinical significance of abnormal hematologic indices in compensated cirrhosisClin Gastroenterol Hepatol20097668969519281860
  • BashourFNTeranJCMullenKDPrevalence of peripheral blood cytopenias (hypersplenism) in patients with nonalcoholic chronic liver diseaseAm J Gastroenterol200095102936293911051371
  • SheikhMYRaoufiRAtlaPRPrevalence of cirrhosis in patients with thrombocytopenia who receive bone marrow biopsySaudi J Gastroenterol201218425726222824769
  • PoynardTBedossaPAge and platelet count: a simple index for predicting the presence of histological lesions in patients with antibodies to hepatitis C virus. METAVIR and CLINIVIR Cooperative Study GroupsJ Viral Hepat1997431992089181529
  • HayashiHBeppuTShirabeKManagement of thrombocytopenia due to liver cirrhosis: a reviewWorld J Gastroenterol201420102595260524627595
  • AsterRHPooling of platelets in the spleen: role in the pathogenesis of “hypersplenic” thrombocytopeniaJ Clin Invest19664556456575327481
  • WendlingFTambourinPThe oncogene V-MPL, a putative truncated cytokine receptor which immortalizes hematopoietic progenitorsNouv Rev Fr Hematol19913321451461662802
  • VigonIMornonJPCocaultLMolecular cloning and characterization of MPL, the human homolog of the v-mpl oncogene: identification of a member of the hematopoietic growth factor receptor superfamilyProc Natl Acad Sci U S A19928912564056441608974
  • MethiaNLouacheFVainchenkerWOligodeoxynucleotides antisense to the proto-oncogene c-mpl specifically inhibit in vitro megakaryocytopoiesisBlood1993825139514017689867
  • LokSKaushanskyKHollyRDCloning and expression of murine thrombopoietin cDNA and stimulation of platelet production in vivoNature199436964815655688202158
  • de SauvageFJHassPESpencerSDStimulation of megakaryocytopoiesis and thrombopoiesis by the c-Mpl ligandNature199436964815335388202154
  • StoffelRWiestnerASkodaRCThrombopoietin in thrombocytopenic mice: evidence against regulation at the mRNA level and for a direct regulatory role of plateletsBlood19968725675738555478
  • FielderPJGurneyALStefanichERegulation of thrombopoietin levels by c-mpl-mediated binding to plateletsBlood1996876215421618630374
  • SaurSJSangkhaeVGeddisAEUbiquitination and degradation of the thrombopoietin receptor c-MplBlood201011561254126319880496
  • SattlerMDurstinMAFrankDAThe thrombopoietin receptor c-MPL activates JAK2 and TYK2 tyrosine kinasesExp Hematol1995239104010487543416
  • RouyezMCBoucheronCGisselbrechtSControl of thrombopoietin-induced megakaryocytic differentiation by the mitogen-activated protein kinase pathwayMol Cell Biol1997179499150009271377
  • GurneyALCarver-MooreKde SauvageFJThrombocytopenia in c-mpl-deficient miceScience19942655177144514478073287
  • KawasakiTTakeshitaASoudaKSerum thrombopoietin levels in patients with chronic hepatitis and liver cirrhosisAm J Gastroenterol19999471918192210406260
  • GianniniEBottaFBorroPRelationship between thrombopoietin serum levels and liver function in patients with chronic liver disease related to hepatitis C virus infectionAm J Gastroenterol200398112516252014638357
  • Peck-RadosavljevicMZacherlJMengYGIs inadequate thrombopoietin production a major cause of thrombocytopenia in cirrhosis of the liver?J Hepatol19972711271319252085
  • MartinTG3rdSombergKAMengYGThrombopoietin levels in patients with cirrhosis before and after orthotopic liver transplantationAnn Intern Med199712742852889265428
  • KoikeYYoneyamaAShiraiJEvaluation of thrombopoiesis in thrombocytopenic disorders by simultaneous measurement of reticulated platelets of whole blood and serum thrombopoietin concentrationsThromb Haemost1998796110611109657432
  • ZeldisJBMugishimaHSteinbergHNIn vitro hepatitis B virus infection of human bone marrow cellsJ Clin Invest19867824114173090103
  • WangCSYaoWJWangSTStrong association of hepatitis C virus (HCV) infection and thrombocytopenia: implications from a survey of a community with hyperendemic HCV infectionClin Infect Dis200439679079615472809
  • BordinGBallareMZigrossiPA laboratory and thrombokinetic study of HCV-associated thrombocytopenia: a direct role of HCV in bone marrow exhaustion?Clin Exp Rheumatol199513Suppl 13S39S438730475
  • Garcia-SuarezJBurgaletaCHernanzNHCV-associated thrombocytopenia: clinical characteristics and platelet response after recombinant alpha2b-interferon therapyBr J Haematol200011019810310930984
  • LindenbaumJLieberCSHematologic effects of alcohol in man in the absence of nutritional deficiencyN Engl J Med196928173333385794307
  • CowanDHHinesJDThrombocytopenia of severe alcoholismAnn Intern Med197174137435539275
  • GrossSKeeferVNewmanAJThe platelets in iron-deficiency anemia. I. The response to oral and parenteral ironPediatrics19643431532314211098
  • EvstatievRBukatyAJimenezKIron deficiency alters megakaryopoiesis and platelet phenotype independent of thrombopoietinAm J Hematol201489552452924464533
  • ChoiSISimoneJVPlatelet production in experimental iron deficiency anemiaBlood19734222192284793111
  • de KlerkGRosengartenPCVetRJSerum erythropoietin (EST) titers in anemiaBlood1981586116411707306704
  • LooMBeguinYThe effect of recombinant human erythropoietin on platelet counts is strongly modulated by the adequacy of iron supplyBlood199993103286329310233880
  • ParkCHValoreEVWaringAJHepcidin, a urinary antimicrobial peptide synthesized in the liverJ Biol Chem2001276117806781011113131
  • NemethETuttleMSPowelsonJHepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalizationScience200430657042090209315514116
  • PigeonCIlyinGCourselaudBA new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overloadJ Biol Chem2001276117811781911113132
  • GeddisAEKaushanskyKCross-reactivity between erythropoietin and thrombopoietin at the level of Mpl does not account for the thrombocytosis seen in iron deficiencyJ Pediatr Hematol Oncol20032511919920 author reply 92014608207
  • RoettoAPapanikolaouGPolitouMMutant antimicrobial peptide hepcidin is associated with severe juvenile hemochromatosisNat Genet2003331212212469120
  • DeugnierYTurlinBle QuilleucDA reappraisal of hepatic siderosis in patients with end-stage cirrhosis: practical implications for the diagnosis of hemochromatosisAm J Surg Pathol19972166696759199645
  • JaroszewiczJRogalskaMFlisiakRSerum prohepcidin reflects the degree of liver function impairment in liver cirrhosisBiomarkers200813547848518979640
  • AllenDWManningNAbnormal phospholipid metabolism in spur cell anemia: decreased fatty acid incorporation into phosphatidylethanolamine and increased incorporation into acylcarnitine in spur cell anemia erythrocytesBlood1994844128312878049442
  • PascoeAKerlinPSteadmanCSpur cell anaemia and hepatic iron stores in patients with alcoholic liver disease undergoing orthotopic liver transplantationGut199945230130510403746
  • ConnellWRKammMARitchieJKBone marrow toxicity caused by azathioprine in inflammatory bowel disease: 27 years of experienceGut1993348108110858174958
  • DuttaTKBadheBACiprofloxacin-induced bone marrow depressionPostgrad Med J19997588757157310616701
  • YamaneANakamuraTSuzukiHInterferon-alpha 2b-induced thrombocytopenia is caused by inhibition of platelet production but not proliferation and endomitosis in human megakaryocytesBlood2008112354255018523149
  • SataMYanoYYoshiyamaYMechanisms of thrombocytopenia induced by interferon therapy for chronic hepatitis BJ Gastroenterol19973222062109085169
  • Peck-RadosavljevicMWichlasMPidlichJBlunted thrombopoietin response to interferon alfa-induced thrombocytopenia during treatment for hepatitis CHepatology1998285142414299794931
  • JandlJHAsterRHIncreased splenic pooling and the pathogenesis of hypersplenismAm J Med Sci196725343833985336447
  • MorrisPWPattonTBBalintJAPortal hypertension, congestive splenomegaly, and portacaval shuntGastroenterology19624255555914476275
  • RiosRSangroBHerreroIThe role of thrombopoietin in the thrombocytopenia of patients with liver cirrhosisAm J Gastroenterol200510061311131615929762
  • SiedleckiCALestiniBJKottke-MarchantKKShear-dependent changes in the three-dimensional structure of human von Willebrand factorBlood1996888293929508874190
  • AryaMAnvariBRomoGMUltralarge multimers of von Willebrand factor form spontaneous high-strength bonds with the platelet glycoprotein Ib-IX complex: studies using optical tweezersBlood200299113971397712010796
  • LianECPathogenesis of thrombotic thrombocytopenic purpura: ADAMTS13 deficiency and beyondSemin Thromb Hemost200531662563216388413
  • TsaiHMPhysiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ionBlood19968710423542448639782
  • RuggeriZMMechanisms of shear-induced platelet adhesion and aggregationThromb Haemost19937011191238236086
  • UemuraMFujimuraYMatsumotoMComprehensive analysis of ADAMTS13 in patients with liver cirrhosisThromb Haemost20089961019102918521503
  • UemuraMFujimuraYKoSPivotal role of ADAMTS13 function in liver diseasesInt J Hematol2010911202920054668
  • OdaAMiyakawaYDrukerBJThrombopoietin primes human platelet aggregation induced by shear stress and by multiple agonistsBlood19968711466446708639835
  • PereiraJAccatinoLAlfaroJPlatelet autoantibodies in patients with chronic liver diseaseAm J Hematol19955031731787485078
  • SanjoASatoiJOhnishiARole of elevated platelet-associated immunoglobulin G and hypersplenism in thrombocytopenia of chronic liver diseasesJ Gastroenterol Hepatol200318663864412753144
  • AokiYHiraiKTanikawaKMechanism of thrombocytopenia in liver cirrhosis: kinetics of indium-111 tropolone labelled plateletsEur J Nucl Med19932021231298440268
  • MacchiLClofent-SanchezGMaritGPAICA: a method for characterizing platelet-associated antibodies – its application to the study of idiopathic thrombocytopenic purpura and to the detection of platelet-bound c7E3Thromb Haemost1996766102010298972027
  • van LeeuwenEFvan der VenJTEngelfrietCPSpecificity of autoantibodies in autoimmune thrombocytopeniaBlood198259123267032627
  • CinesDBBlanchetteVSImmune thrombocytopenic purpuraN Engl J Med200234613995100811919310
  • GeorgeJNWoolfSHRaskobGEIdiopathic thrombocytopenic purpura: a practice guideline developed by explicit methods for the American Society of HematologyBlood19968813408704187
  • BassendineMFCollinsJDStephensonJPlatelet associated immunoglobulins in primary biliary cirrhosis: a cause of thrombocytopenia?Gut19852610107410794054707
  • ArakawaYAmakiSMiyakawaHPBC-AIH overlap syndrome with concomitant ITP and Hashimoto’s disease with positivity for anti-centromere antibodyJ Gastroenterol200439549049515175950
  • PawlotskyJMBouvierMFromontPHepatitis C virus infection and autoimmune thrombocytopenic purpuraJ Hepatol19952366356398750160
  • ChiaoEYEngelsEAKramerJRRisk of immune thrombocytopenic purpura and autoimmune hemolytic anemia among 120 908 US veterans with hepatitis C virus infectionArch Intern Med2009169435736319237719
  • MisianiRBellavitaPFeniliDHepatitis C virus infection in patients with essential mixed cryoglobulinemiaAnn Intern Med199211775735771326246
  • SteeperTAHorwitzCAMooreSBSevere thrombocytopenia in Epstein-Barr virus-induced mononucleosisWest J Med198915021701732543142
  • WekslerBBReview article: the pathophysiology of thrombocytopenia in hepatitis C virus infection and chronic liver diseaseAliment Pharmacol Ther200726Suppl 1131917958515
  • MayoMJExtrahepatic manifestations of hepatitis C infectionAm J Med Sci2003325313514812640289
  • NagamineTOhtukaTTakeharaKThrombocytopenia associated with hepatitis C viral infectionJ Hepatol19962421351408907565
  • HamaiaSLiCAllainJPThe dynamics of hepatitis C virus binding to platelets and 2 mononuclear cell linesBlood20019882293230011588022
  • PanzerSSeelEIs there an increased frequency of autoimmune thrombocytopenia in hepatitis C infection? A reviewWien Med Wochenschr200315319–2041742014648921
  • VisentinGPLiuCYDrug-induced thrombocytopeniaHematol Oncol Clin North Am2007214685696vi17666285
  • GeorgeJNRaskobGEShahSRDrug-induced thrombocytopenia: a systematic review of published case reportsAnn Intern Med1998129118868909867731
  • DourakisSPDeutschMHadziyannisSJImmune thrombocytopenia and alpha-interferon therapyJ Hepatol19962569729759007728
  • ArenaRCecinatoPLisottiASevere immune thrombocytopenia after peg-interferon-alpha2a, ribavirin and telaprevir treatment completion: a case report and systematic review of literatureWorld J Hepatol20157121718172226140092
  • AlberioLKimmerleSBaumannARapid determination of anti-heparin/platelet factor 4 antibody titers in the diagnosis of heparin-induced thrombocytopeniaAm J Med2003114752853612753876
  • NewmanPMChongBHHeparin-induced thrombocytopenia: new evidence for the dynamic binding of purified anti-PF4-heparin antibodies to platelets and the resultant platelet activationBlood200096118218710891449
  • AsterRHBougieDWDrug-induced immune thrombocytopeniaN Engl J Med2007357658058717687133
  • WarkentinTEDrug-induced immune-mediated thrombocytopenia – from purpura to thrombosisN Engl J Med2007356989189317329695
  • WimanBCollenDMolecular mechanism of physiological fibrinolysisNature19782725653549550151233
  • HerschSLKunelisTFrancisRBJrThe pathogenesis of accelerated fibrinolysis in liver cirrhosis: a critical role for tissue plasminogen activator inhibitorBlood1987695131513192436684
  • CollenDIdentification and some properties of a new fast-reacting plasmin inhibitor in human plasmaEur J Biochem1976691209216136345
  • BajzarLThrombin activatable fibrinolysis inhibitor and an antifibrinolytic pathwayArterioscler Thromb Vasc Biol200020122511251811116046
  • LeiperKCrollABoothNATissue plasminogen activator, plasminogen activator inhibitors, and activator-inhibitor complex in liver diseaseJ Clin Pathol19944732142178163691
  • Van ThielDHGeorgeMFareedJLow levels of thrombin activatable fibrinolysis inhibitor (TAFI) in patients with chronic liver diseaseThromb Haemost200185466767011341503
  • KujovichJLHemostatic defects in end stage liver diseaseCrit Care Clin200521356358715992673
  • SteinSFHarkerLAKinetic and functional studies of platelets, fibrinogen, and plasminogen in patients with hepatic cirrhosisJ Lab Clin Med19829922172307061918
  • IkuraYOhsawaMOkadaMThe significance of platelet consumption in the development of thrombocytopenia in patients with cirrhosisAm J Med Sci2013346319920323979210
  • BoylanJFKlinckJRSandlerANTranexamic acid reduces blood loss, transfusion requirements, and coagulation factor use in primary orthotopic liver transplantationAnesthesiology199685510431048 discussion 1030A–1031A8916821
  • PorteRJMolenaarIQBegliominiBAprotinin and transfusion requirements in orthotopic liver transplantation: a multicentre randomised double-blind study. EMSALT Study GroupLancet200035592121303130910776742
  • DalmauASabateAKooMThe prophylactic use of tranexamic acid and aprotinin in orthotopic liver transplantation: a comparative studyLiver Transpl200410227928414762867
  • GunawanBRunyonBThe efficacy and safety of epsilon-aminocaproic acid treatment in patients with cirrhosis and hyperfibrinolysisAliment Pharmacol Ther200623111512016393288
  • LumsdenABHendersonJMKutnerMHEndotoxin levels measured by a chromogenic assay in portal, hepatic and peripheral venous blood in patients with cirrhosisHepatology1988822322363281884
  • KalambokisGTsianosEVEndotoxaemia in the pathogenesis of cytopenias in liver cirrhosis. Could oral antibiotics raise blood counts?Med Hypotheses201176110510920832949
  • WiestRGarcia-TsaoGBacterial translocation (BT) in cirrhosisHepatology200541342243315723320
  • KuratsuneHKodaTKurahoriTThe relationship between endotoxin and the phagocytic activity of the reticuloendothelial systemHepatogastroenterology198330379826193047
  • Garcia-TsaoGWiestRGut microflora in the pathogenesis of the complications of cirrhosisBest Pract Res Clin Gastroenterol200418235337215123075
  • DeviereJContentJDenysCExcessive in vitro bacterial lipopolysaccharide-induced production of monokines in cirrhosisHepatology19901146286342184115
  • LinRSLeeFYLeeSDEndotoxemia in patients with chronic liver diseases: relationship to severity of liver diseases, presence of esophageal varices, and hyperdynamic circulationJ Hepatol19952221651727790704
  • KalambokisGNMouzakiARodiMRifaximin improves thrombocytopenia in patients with alcoholic cirrhosis in association with reduction of endotoxaemiaLiver Int201232346747522098272
  • ItohHCicalaCDouglasGJPlatelet accumulation induced by bacterial endotoxin in ratsThromb Res19968364054198885136
  • PanasiukAZakJKasprzyckaEBlood platelet and monocyte activations and relation to stages of liver cirrhosisWorld J Gastroenterol200511182754275815884116
  • JelkmannWWolffMFandreyJModulation of the production of erythropoietin by cytokines: in vitro studies and their clinical implicationsContrib Nephrol19908768772128766
  • LiJXiaYBertinoAMThe mechanism of apoptosis in human platelets during storageTransfusion200040111320132911099659
  • NathanCNitric oxide as a secretory product of mammalian cellsFASEB J1992612305130641381691
  • SchobersbergerWHoffmannGFandreyJNitric oxide donors suppress erythropoietin production in vitroPflugers Arch199643269809858781191
  • GustotTDurandFLebrecDSevere sepsis in cirrhosisHepatology20095062022203319885876
  • VenkataCKashyapRFarmerJCThrombocytopenia in adult patients with sepsis: incidence, risk factors, and its association with clinical outcomeJ Intensive Care201311925810916
  • CalyWRStraussEA prospective study of bacterial infections in patients with cirrhosisJ Hepatol19931833533588228129
  • ForemanMGManninoDMMossMCirrhosis as a risk factor for sepsis and death: analysis of the National Hospital Discharge SurveyChest200312431016102012970032
  • WangYQWangBLiangYRole of platelet TLR4 expression in pathogensis of septic thrombocytopeniaWorld J Emerg Med201121131725214976
  • GawazMDickfeldTBognerCPlatelet function in septic multiple organ dysfunction syndromeIntensive Care Med19972343793859142575
  • PignatelliPDe BiaseLLentiLTumor necrosis factor-alpha as trigger of platelet activation in patients with heart failureBlood200510661992199415956282
  • WarkentinTEAirdWCRandJHPlatelet-endothelial interactions: sepsis, HIT, and antiphospholipid syndromeHematology Am Soc Hematol Educ Program200349751914633796
  • KalambokisGTsianosEVThrombocytopenia associated with chronic liver disease: effects of rifaximin on platelet countAm J Gastroenterol2010105122705270721131941
  • KrauelKHackbarthCFurllBHeparin-induced thrombocytopenia: in vitro studies on the interaction of dabigatran, rivaroxaban, and low-sulfated heparin, with platelet factor 4 and anti-PF4/heparin antibodiesBlood201211951248125522049520
  • PongasGDasguptaSKThiagarajanPAntiplatelet factor 4/heparin antibodies in patients with gram negative bacteremiaThromb Res2013132221722023830968
  • MontaltoPVlachogiannakosJCoxDJBacterial infection in cirrhosis impairs coagulation by a heparin effect: a prospective studyJ Hepatol200237446347012217599
  • Spleen [webpage on the Internet]Redondo Beach, CAPacific Health and Wellness2014 Available from: http://phaws.com/spleen/Accessed February 18, 2016
  • Liver and Cirrhosis [webpage on the Internet]Seattle, WACognition Studio Available from: http://cognitionstudio.com/Accessed March 23, 2016