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Semin Thromb Hemost 2011; 37(8): 946-954
DOI: 10.1055/s-0031-1297373
© Thieme Medical Publishers

Thrombosis and Occlusion of Vascular Access in Hemodialyzed Patients

Martina Montagnana1 , Tiziana Meschi2 , Loris Borghi2 , Giuseppe Lippi3
  • 1Sezione di Biochimica Clinica, Dipartimento di Scienze della Vita e della Riproduzione, Università degli Studi di Verona
  • 2Sezione di Medicina Interna e Lungodegenza Critica, Dipartimento di Scienze Cliniche, Azienda Ospedaliero-Universitaria di Parma, Parma
  • 3U.O. Diagnostica Ematochimica, Dipartimento di Patologia e Medicina di Laboratorio, Azienda Ospedaliero-Universitaria di Parma, Italy
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Publication History

Publication Date:
23 December 2011 (online)

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ABSTRACT

Patients undergoing chronic hemodialysis have a high risk of arterial thrombotic events as well as vascular access thrombosis (VAT). The latter complication has been consistently associated with inherited (i.e., the prothrombin 20210 polymorphism, and polymorphisms in the genes encoding for transforming growth factor-β1, nitric oxide synthase, plasminogen activator inhibitor-1, angiotensin converting enzyme, and methylene tetrahydrofolate reductase), and acquired thrombotic risk factors (i.e., diabetes, obesity, atrial fibrillation, hypertension, hyperhomocysteinemia, hyperlipoproteinemia(a), low serum albumin, antiphospholipid antibodies, autoantibodies against protein C and S, erythropoietin administration, malnutrition, and cytomegalovirus infection). The three main factors involved in the pathogenesis of VAT overlap those of venous thrombosis and therefore include endothelial cell injury, blood stasis, and hypercoagulability. These changes are characteristic of patients affected by end-stage renal disease and might be further aggravated during and after hemodialysis. The aim of this review is to describe the epidemiology and pathogenesis of thrombosis of dialysis vascular access and to discuss the application of therapeutic interventions in prevention and treatment of this clinical problem.

KEYWORDS

Hemodialysis - thrombotic events - arteriovenous fistula - stenosis - vascular access thrombosis

REFERENCES

  • 1 Lindner A, Charra B, Sherrard D J, Scribner B H. Accelerated atherosclerosis in prolonged maintenance hemodialysis.  N Engl J Med. 1974;  290 (13) 697-701
    Search in Google Scholar
  • 2 Winkelmayer W C. Tackling the Achilles' heel of hemodialysis.  N Engl J Med. 2011;  364 (4) 372-374
    Search in Google Scholar
  • 3 Swartz R D, Messana J M, Boyer C J, Lunde N M, Weitzel W F, Hartman T L. Successful use of cuffed central venous hemodialysis catheters inserted percutaneously.  J Am Soc Nephrol. 1994;  4 (9) 1719-1725
    Search in Google Scholar
  • 4 Trerotola S O, Johnson M S, Harris V J et al.. Outcome of tunneled hemodialysis catheters placed via the right internal jugular vein by interventional radiologists.  Radiology. 1997;  203 (2) 489-495
    Search in Google Scholar
  • 5 Li L, Terry C M, Shiu Y T, Cheung A K. Neointimal hyperplasia associated with synthetic hemodialysis grafts.  Kidney Int. 2008;  74 (10) 1247-1261
    Search in Google Scholar
  • 6 Akoh J A. Prosthetic arteriovenous grafts for hemodialysis.  J Vasc Access. 2009;  10 (3) 137-147
    Search in Google Scholar
  • 7 Murad M H, Elamin M B, Sidawy A N et al.. Autogenous versus prosthetic vascular access for hemodialysis: a systematic review and meta-analysis.  J Vasc Surg. 2008;  48 (5, Suppl) 34S-47S
    Search in Google Scholar
  • 8 National Kidney Foundation-Dialysis Outcomes Quality Initiative . NKF-DOQI clinical practice guidelines for vascular access.  Am J Kidney Dis. 1997;  30 (4, Suppl 3) S150-S191
    Search in Google Scholar
  • 9 Papanikolaou V, Papagiannis A, Vrochides D et al.. The natural history of vascular access for hemodialysis: a single center study of 2,422 patients.  Surgery. 2009;  145 (3) 272-279
    Search in Google Scholar
  • 10 Huber T S, Carter J W, Carter R L, Seeger J M. Patency of autogenous and polytetrafluoroethylene upper extremity arteriovenous hemodialysis accesses: a systematic review.  J Vasc Surg. 2003;  38 (5) 1005-1011
    Search in Google Scholar
  • 11 Gibson K D, Gillen D L, Caps M T, Kohler T R, Sherrard D J, Stehman-Breen C O. Vascular access survival and incidence of revisions: a comparison of prosthetic grafts, simple autogenous fistulas, and venous transposition fistulas from the United States Renal Data System Dialysis Morbidity and Mortality Study.  J Vasc Surg. 2001;  34 (4) 694-700
    Search in Google Scholar
  • 12 Gilpin V, Nichols W K. Vascular access for hemodialysis: thrills and thrombosis.  J Vasc Nurs. 2010;  28 (2) 78-83
    Search in Google Scholar
  • 13 Kherlakian G M, Roedersheimer L R, Arbaugh J J, Newmark K J, King L R. Comparison of autogenous fistula versus expanded polytetrafluoroethylene graft fistula for angioaccess in hemodialysis.  Am J Surg. 1986;  152 (2) 238-243
    Search in Google Scholar
  • 14 Tordoir J H, Herman J M, Kwan T S, Diderich P M. Long-term follow-up of the polytetrafluoroethylene (PTFE) prosthesis as an arteriovenous fistula for haemodialysis.  Eur J Vasc Surg. 1988;  2 (1) 3-7
    Search in Google Scholar
  • 15 Ascher E, Gade P, Hingorani A et al.. Changes in the practice of angioaccess surgery: impact of dialysis outcome and quality initiative recommendations.  J Vasc Surg. 2000;  31 (1 Pt 1) 84-92
    Search in Google Scholar
  • 16 Ponikvar R, Buturović-Ponikvar J. Temporary hemodialysis catheters as a long-term vascular access in chronic hemodialysis patients.  Ther Apher Dial. 2005;  9 (3) 250-253
    Search in Google Scholar
  • 17 Blankestijn P. Cuffed tunneled catheters for long-term vascular access. In: Conlon P J, Nicholson M, Schwab S, eds. Hemodialysis Vascular Access: Practice and Problems. New York: Oxford University; 2004: 67-84
    Search in Google Scholar
  • 18 Moureau N, Poole S, Murdock M A, Gray S M, Semba C P. Central venous catheters in home infusion care: outcomes analysis in 50,470 patients.  J Vasc Interv Radiol. 2002;  13 (10) 1009-1016
    Search in Google Scholar
  • 19 Agarwal A K. Central vein stenosis: current concepts.  Adv Chronic Kidney Dis. 2009;  16 (5) 360-370
    Search in Google Scholar
  • 20 Agarwal A K, Patel B M, Haddad N J. Central vein stenosis: a nephrologist's perspective.  Semin Dial. 2007;  20 (1) 53-62
    Search in Google Scholar
  • 21 Lippi G, Franchini M. Pathogenesis of venous thromboembolism: when the cup runneth over.  Semin Thromb Hemost. 2008;  34 (8) 747-761
    Search in Google Scholar
  • 22 Lippi G, Franchini M, Favaloro E J. Unsuspected triggers of venous thromboembolism—trivial or not so trivial?.  Semin Thromb Hemost. 2009;  35 (7) 597-604
    Search in Google Scholar
  • 23 Montagnana M, Favaloro E J, Franchini M, Guidi G C, Lippi G. The role of ethnicity, age and gender in venous thromboembolism.  J Thromb Thrombolysis. 2010;  29 (4) 489-496
    Search in Google Scholar
  • 24 Casserly L F, Dember L M. Thrombosis in end-stage renal disease.  Semin Dial. 2003;  16 (3) 245-256
    Search in Google Scholar
  • 25 Paulson W D. Prediction of hemodialysis synthetic graft thrombosis: can we identify factors that impair validity of the dysfunction hypothesis?.  Am J Kidney Dis. 2000;  35 (5) 973-975
    Search in Google Scholar
  • 26 Brophy D F, Bukaveckas B L, Ferreira-Gonzalez A, Archer K J, Martin E J, Gehr T W. A pilot study of genetic polymorphisms and hemodialysis vascular access thrombosis.  Hemodial Int. 2009;  13 (1) 19-26
    Search in Google Scholar
  • 27 Knoll G A, Wells P S, Young D et al.. Thrombophilia and the risk for hemodialysis vascular access thrombosis.  J Am Soc Nephrol. 2005;  16 (4) 1108-1114
    Search in Google Scholar
  • 28 Ataç B, Yakupoğlu U, Ozbek N, Ozdemir F N, Bilgin N. Role of genetic mutations in vascular access thrombosis among hemodialysis patients waiting for renal transplantation.  Transplant Proc. 2002;  34 (6) 2030-2032
    Search in Google Scholar
  • 29 Bremer C, Schaefer R M. Heterozygosity for factor V Leiden in a haemodialysis patient with recurrent shunt thrombosis.  Nephrol Dial Transplant. 1997;  12 (8) 1775-1776
    Search in Google Scholar
  • 30 Rios D R, Fernandes A P, Carvalho M G et al.. Hemodialysis vascular access thrombosis: The role of factor V Leiden, prothrombin gene mutation and ABO blood groups.  Clin Chim Acta. 2011;  412 (5-6) 425-429
    Search in Google Scholar
  • 31 Födinger M, Mannhalter C, Pabinger I et al.. Resistance to activated protein C (APC): mutation at Arg506 of coagulation factor V and vascular access thrombosis in haemodialysis patients.  Nephrol Dial Transplant. 1996;  11 (4) 668-672
    Search in Google Scholar
  • 32 Fekih-Mrissa N, Klai S, Bafoun A, Nciri B, Hmida J, Gritli N. Role of thrombophilia in vascular access thrombosis among chronic hemodialysis patients in Tunisia.  Ther Apher Dial. 2011;  15 (1) 40-43
    Search in Google Scholar
  • 33 Heine G H, Ulrich C, Sester U, Sester M, Köhler H, Girndt M. Transforming growth factor beta1 genotype polymorphisms determine AV fistula patency in hemodialysis patients.  Kidney Int. 2003;  64 (3) 1101-1107
    Search in Google Scholar
  • 34 Girndt M, Heine G H, Ulrich C, Köhler H. DialGene Consortium . Gene polymorphism association studies in dialysis: vascular access.  Semin Dial. 2007;  20 (1) 63-67
    Search in Google Scholar
  • 35 Stracke S, Konner K, Köstlin I et al.. Increased expression of TGF-beta1 and IGF-I in inflammatory stenotic lesions of hemodialysis fistulas.  Kidney Int. 2002;  61 (3) 1011-1019
    Search in Google Scholar
  • 36 Lazo-Langner A, Knoll G A, Wells P S, Carson N, Rodger M A. The risk of dialysis access thrombosis is related to the transforming growth factor-beta1 production haplotype and is modified by polymorphisms in the plasminogen activator inhibitor-type 1 gene.  Blood. 2006;  108 (13) 4052-4058
    Search in Google Scholar
  • 37 Sung S A, Ko G J, Jo S K, Cho W Y, Kim H K, Lee S Y. Interleukin-10 and tumor necrosis factor-alpha polymorphisms in vascular access failure in patients on hemodialysis: preliminary data in Korea.  J Korean Med Sci. 2008;  23 (1) 89-93
    Search in Google Scholar
  • 38 Basaran O, Atac F B, Karakayali F et al.. Endothelial nitric oxide synthase gene intron 4 (VNTR) polymorphism and vascular access graft thrombosis.  J Invest Surg. 2007;  20 (1) 49-53
    Search in Google Scholar
  • 39 Trimarchi H, Duboscq C, Genoud V et al.. Plasminogen activator inhibitor-1 activity and 4G/5G polymorphism in hemodialysis.  J Vasc Access. 2008;  9 (2) 142-147
    Search in Google Scholar
  • 40 Güngör Y, Kayataş M, Yıldız G, Özdemir Ö, Candan F. The presence of PAI-1 4G/5G and ACE DD genotypes increases the risk of early-stage AVF thrombosis in hemodialysis patients.  Ren Fail. 2011;  33 (2) 169-175
    Search in Google Scholar
  • 41 Rigat B, Hubert C, Alhenc-Gelas F, Cambien F, Corvol P, Soubrier F. An insertion/deletion polymorphism in the angiotensin I-converting enzyme gene accounting for half the variance of serum enzyme levels.  J Clin Invest. 1990;  86 (4) 1343-1346
    Search in Google Scholar
  • 42 Sajgure A, Choudhury A, Ahmed Z, Choudhury D. Angiotensin converting enzyme inhibitors maintain polytetrafluroethylene graft patency.  Nephrol Dial Transplant. 2007;  22 (5) 1390-1398
    Search in Google Scholar
  • 43 Heine G H, Ulrich C, Köhler H, Girndt M. Is AV fistula patency associated with angiotensin-converting enzyme (ACE) polymorphism and ACE inhibitor intake?.  Am J Nephrol. 2004;  24 (4) 461-468
    Search in Google Scholar
  • 44 Molino D, De Lucia D, Marotta R et al.. In uremia, plasma levels of anti-protein C and anti-protein S antibodies are associated with thrombosis.  Kidney Int. 2005;  68 (3) 1223-1229
    Search in Google Scholar
  • 45 Windus D W, Jendrisak M D, Delmez J A. Prosthetic fistula survival and complications in hemodialysis patients: effects of diabetes and age.  Am J Kidney Dis. 1992;  19 (5) 448-452
    Search in Google Scholar
  • 46 Chou C Y, Chen J Y, Liu J H et al.. Atrial fibrillation linked to vascular access thrombosis in chronic hemodialysis patients.  J Atheroscler Thromb. 2011;  18 (6) 448-453
    Search in Google Scholar
  • 47 Erkut B, Unlü Y, Ceviz M et al.. Primary arteriovenous fistulas in the forearm for hemodialysis: effect of miscellaneous factors in fistula patency.  Ren Fail. 2006;  28 (4) 275-281
    Search in Google Scholar
  • 48 Obialo C I, Robinson T, Brathwaite M. Hemodialysis vascular access: variable thrombus-free survival in three subpopulations of black patients.  Am J Kidney Dis. 1998;  31 (2) 250-256
    Search in Google Scholar
  • 49 Moustapha A, Naso A, Nahlawi M et al.. Prospective study of hyperhomocysteinemia as an adverse cardiovascular risk factor in end-stage renal disease.  Circulation. 1998;  97 (2) 138-141
    Search in Google Scholar
  • 50 Fermo I, Vigano' D'Angelo S, Paroni R, Mazzola G, Calori G, D'Angelo A. Prevalence of moderate hyperhomocysteinemia in patients with early-onset venous and arterial occlusive disease.  Ann Intern Med. 1995;  123 (10) 747-753
    Search in Google Scholar
  • 51 Zoccali C, Mallamaci F, Tripepi G. It is important to lower homocysteine in dialysis patients.  Semin Dial. 2007;  20 (6) 530-533
    Search in Google Scholar
  • 52 Mallamaci F, Bonanno G, Seminara G et al.. Hyperhomocysteinemia and arteriovenous fistula thrombosis in hemodialysis patients.  Am J Kidney Dis. 2005;  45 (4) 702-707
    Search in Google Scholar
  • 53 Churchill D N, Taylor D W, Cook R J et al.. Canadian hemodialysis morbidity study.  Am J Kidney Dis. 1992;  19 (3) 214-234
    Search in Google Scholar
  • 54 Molino D, De Santo N G, Marotta R, Anastasio P, Mosavat M, De Lucia D. Plasma levels of plasminogen activator inhibitor type 1, factor VIII, prothrombin activation fragment 1 + 2, anticardiolipin, and antiprothrombin antibodies are risk factors for thrombosis in hemodialysis patients.  Semin Nephrol. 2004;  24 (5) 495-501
    Search in Google Scholar
  • 55 Goldwasser P, Michel M A, Collier J et al.. Prealbumin and lipoprotein(a) in hemodialysis: relationships with patient and vascular access survival.  Am J Kidney Dis. 1993;  22 (1) 215-225
    Search in Google Scholar
  • 56 Chou C Y, Kuo H L, Yung Y F, Liu Y L, Huang C C. C-reactive protein predicts vascular access thrombosis in hemodialysis patients.  Blood Purif. 2006;  24 (4) 342-346
    Search in Google Scholar
  • 57 Muirhead N, Laupacis A, Wong C. Erythropoietin for anemia in hemodialysis patients: Results of a maintenance study.  Nephrol Dial Transplant. 1992;  7 811-816
    Search in Google Scholar
  • 58 al-Momen A K, Huraib S O, Gader A M, Sulaimani F. Low dose danazol is effective in management of erythropoietin induced thrombosis.  Thromb Res. 1991;  64 (5) 527-532
    Search in Google Scholar
  • 59 Lee Y K, Koo J R, Kim J K et al.. Effect of route of EPO administration on hemodialysis arteriovenous vascular access failure: a randomized controlled trial.  Am J Kidney Dis. 2009;  53 (5) 815-822
    Search in Google Scholar
  • 60 Canadian Erythropoietin Study Group . Association between recombinant human erythropoietin and quality of life and exercise capacity of patients receiving haemodialysis.  BMJ. 1990;  300 (6724) 573-578
    Search in Google Scholar
  • 61 Palmer S C, Navaneethan S D, Craig J C et al.. Meta-analysis: erythropoiesis-stimulating agents in patients with chronic kidney disease.  Ann Intern Med. 2010;  153 (1) 23-33
    Search in Google Scholar
  • 62 Tang I Y, Vrahnos D, Valaitis D, Lau A H. Vascular access thrombosis during recombinant human erythropoietin therapy.  ASAIO J. 1992;  38 (3) M528-M531
    Search in Google Scholar
  • 63 Standage B A, Schuman E S, Ackerman D, Gross G F, Ragsdale J W. Does the use of erythropoietin in hemodialysis patients increase dialysis graft thrombosis rates?.  Am J Surg. 1993;  165 (5) 650-654
    Search in Google Scholar
  • 64 Brunet P, Aillaud M F, San Marco M et al.. Antiphospholipids in hemodialysis patients: relationship between lupus anticoagulant and thrombosis.  Kidney Int. 1995;  48 (3) 794-800
    Search in Google Scholar
  • 65 Prakash R, Miller III C C, Suki W N. Anticardiolipin antibody in patients on maintenance hemodialysis and its association with recurrent arteriovenous graft thrombosis.  Am J Kidney Dis. 1995;  26 (2) 347-352
    Search in Google Scholar
  • 66 Prieto L N, Suki W N. Frequent hemodialysis graft thrombosis: association with antiphospholipid antibodies.  Am J Kidney Dis. 1994;  23 (4) 587-590
    Search in Google Scholar
  • 67 Shalhoub R J. Pathogenesis of lipoid nephrosis: a disorder of T-cell function.  Lancet. 1974;  2 (7880) 556-560
    Search in Google Scholar
  • 68 Gültekin F, Alagözlü H, Candan F, Nadir I, Bakici M Z, Sezer H. The relationship between anticardiolipin antibodies and vascular access occlusion in patients on hemodialysis.  ASAIO J. 2005;  51 (2) 162-164
    Search in Google Scholar
  • 69 Chuang F R, Chen T C, Yang C C et al.. IgM-anticardiolipin antibody and vascular access thrombosis in chronic hemodialysis patients.  Ren Fail. 2005;  27 (1) 25-30
    Search in Google Scholar
  • 70 Weisinger J R, Kempson R L, Eldridge F L, Swenson R S. The nephrotic syndrome: a complication of massive obesity.  Ann Intern Med. 1974;  81 (4) 440-447
    Search in Google Scholar
  • 71 Cull J D, Cull D L, Taylor S M et al.. Prosthetic thigh arteriovenous access: outcome with SVS/AAVS reporting standards.  J Vasc Surg. 2004;  39 (2) 381-386
    Search in Google Scholar
  • 72 Gagliardi G M, Rossi S, Condino F et al.. Malnutrition, infection and arteriovenous fistula failure: is there a link?.  J Vasc Access. 2011;  12 (1) 57-62
    Search in Google Scholar
  • 73 Lin C C, Yang W C. Prognostic factors influencing the patency of hemodialysis vascular access: literature review and novel therapeutic modality by far infrared therapy.  J Chin Med Assoc. 2009;  72 (3) 109-116
    Search in Google Scholar
  • 74 Himmelfarb J, Stenvinkel P, Ikizler T A, Hakim R M. The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia.  Kidney Int. 2002;  62 (5) 1524-1538
    Search in Google Scholar
  • 75 Malyszko J. Mechanism of endothelial dysfunction in chronic kidney disease.  Clin Chim Acta. 2010;  411 (19-20) 1412-1420
    Search in Google Scholar
  • 76 Roy-Chaudhury P, Kelly B S, Miller M A et al.. Venous neointimal hyperplasia in polytetrafluoroethylene dialysis grafts.  Kidney Int. 2001;  59 (6) 2325-2334
    Search in Google Scholar
  • 77 Weiss M F, Scivittaro V, Anderson J M. Oxidative stress and increased expression of growth factors in lesions of failed hemodialysis access.  Am J Kidney Dis. 2001;  37 (5) 970-980
    Search in Google Scholar
  • 78 Swedberg S H, Brown B G, Sigley R, Wight T N, Gordon D, Nicholls S C. Intimal fibromuscular hyperplasia at the venous anastomosis of PTFE grafts in hemodialysis patients. Clinical, immunocytochemical, light and electron microscopic assessment.  Circulation. 1989;  80 (6) 1726-1736
    Search in Google Scholar
  • 79 Reddy M K, Vasir J K, Hegde G V, Joshi S S, Labhasetwar V. Erythropoietin induces excessive neointima formation: a study in a rat carotid artery model of vascular injury.  J Cardiovasc Pharmacol Ther. 2007;  12 (3) 237-247
    Search in Google Scholar
  • 80 Douzdjian V, Abecassis M M. A new technique of prosthetic arteriovenous fistula construction that eliminates the need for temporary access.  Am J Surg. 1993;  166 (3) 304-305
    Search in Google Scholar
  • 81 Barth C, Boer W, Garzoni D et al.. Characteristics of hypotension-prone haemodialysis patients: is there a critical relative blood volume?.  Nephrol Dial Transplant. 2003;  18 (7) 1353-1360
    Search in Google Scholar
  • 82 Kao C L, Chang J P. Fully ringed polytetrafluoroethylene graft for vascular access in hemodialysis.  Asian Cardiovasc Thorac Ann. 2003;  11 (2) 171-173
    Search in Google Scholar
  • 83 Miller P E, Carlton D, Deierhoi M H, Redden D T, Allon M. Natural history of arteriovenous grafts in hemodialysis patients.  Am J Kidney Dis. 2000;  36 (1) 68-74
    Search in Google Scholar
  • 84 Nampoory M R, Das K C, Johny K V et al.. Hypercoagulability, a serious problem in patients with ESRD on maintenance hemodialysis, and its correction after kidney transplantation.  Am J Kidney Dis. 2003;  42 (4) 797-805
    Search in Google Scholar
  • 85 Ambühl P M, Wüthrich R P, Korte W, Schmid L, Krapf R. Plasma hypercoagulability in haemodialysis patients: impact of dialysis and anticoagulation.  Nephrol Dial Transplant. 1997;  12 (11) 2355-2364
    Search in Google Scholar
  • 86 Milburn J A, Cassar K, Ford I, Fluck N, Brittenden J. Prothrombotic changes in platelet, endothelial and coagulation function following hemodialysis.  Int J Artif Organs. 2011;  34 (3) 280-287
    Search in Google Scholar
  • 87 Schoorl M, Schoorl M, Nubé M J, Bartels P C. Platelet depletion, platelet activation and coagulation during treatment with hemodialysis.  Scand J Clin Lab Invest. 2011;  71 (3) 240-247
    Search in Google Scholar
  • 88 Mercier E, Branger B, Vecina F et al.. Tissue factor coagulation pathway and blood cells activation state in renal insufficiency.  Hematol J. 2001;  2 (1) 18-25
    Search in Google Scholar
  • 89 Spijker H T, Graaff R, Boonstra P W, Busscher H J, van Oeveren W. On the influence of flow conditions and wettability on blood material interactions.  Biomaterials. 2003;  24 (26) 4717-4727
    Search in Google Scholar
  • 90 Jurk K, Kehrel B E. Platelets: physiology and biochemistry.  Semin Thromb Hemost. 2005;  31 (4) 381-392
    Search in Google Scholar
  • 91 Flaumenhaft R, Mairuhu A T, Italiano J E. Platelet- and megakaryocyte-derived microparticles.  Semin Thromb Hemost. 2010;  36 (8) 881-887
    Search in Google Scholar
  • 92 Ando M, Iwata A, Ozeki Y, Tsuchiya K, Akiba T, Nihei H. Circulating platelet-derived microparticles with procoagulant activity may be a potential cause of thrombosis in uremic patients.  Kidney Int. 2002;  62 (5) 1757-1763
    Search in Google Scholar
  • 93 Cianciolo G, Stefoni S, Donati G et al.. Intra- and post-dialytic platelet activation and PDGF-AB release: cellulose diacetate vs polysulfone membranes.  Nephrol Dial Transplant. 2001;  16 (6) 1222-1229
    Search in Google Scholar
  • 94 Gritters-van den Oever M, Schoorl M, Schoorl M, Bartels P C, Grooteman M P, Nubé M J. The role of the extracorporeal circuit in the trapping and degranulation of platelets.  Blood Purif. 2009;  28 (3) 253-259
    Search in Google Scholar
  • 95 Schoorl M, Schoorl M, Bartels P C. Changes in platelet volume, morphology and RNA content in subjects treated with haemodialysis.  Scand J Clin Lab Invest. 2008;  68 (4) 335-342
    Search in Google Scholar
  • 96 Itoh S, Takeshita K, Susuki C, Shige-Eda K, Tsuji T. Redistribution of P-selectin ligands on neutrophil cell membranes and the formation of platelet-neutrophil complex induced by hemodialysis membranes.  Biomaterials. 2008;  29 (21) 3084-3090
    Search in Google Scholar
  • 97 Sirolli V, Ballone E, Di Stante S, Amoroso L, Bonomini M. Cell activation and cellular-cellular interactions during hemodialysis: effect of dialyzer membrane.  Int J Artif Organs. 2002;  25 (6) 529-537
    Search in Google Scholar
  • 98 Frank R D, Weber J, Dresbach H, Thelen H, Weiss C, Floege J. Role of contact system activation in hemodialyzer-induced thrombogenicity.  Kidney Int. 2001;  60 (5) 1972-1981
    Search in Google Scholar
  • 99 Basmadjian D, Sefton M V, Baldwin S A. Coagulation on biomaterials in flowing blood: some theoretical considerations.  Biomaterials. 1997;  18 (23) 1511-1522
    Search in Google Scholar
  • 100 Lucchi L, Ligabue G, Marietta M et al.. Activation of coagulation during hemodialysis: effect of blood lines alone and whole extracorporeal circuit.  Artif Organs. 2006;  30 (2) 106-110
    Search in Google Scholar
  • 101 Kushiya F, Wada H, Sakakura M et al.. Atherosclerotic and hemostatic abnormalities in patients undergoing hemodialysis.  Clin Appl Thromb Hemost. 2003;  9 (1) 53-60
    Search in Google Scholar
  • 102 Vaziri N D, Gonzales E C, Wang J, Said S. Blood coagulation, fibrinolytic, and inhibitory proteins in end-stage renal disease: effect of hemodialysis.  Am J Kidney Dis. 1994;  23 (6) 828-835
    Search in Google Scholar
  • 103 Opatrný Jr K, Vít L, Opatrná S, Sulková S, Bodláková B. [Hypofibrinolysis after venous occlusion in patients treated with long-term hemodialysis].  Cas Lek Cesk. 1994;  133 (11) 346-349
    Search in Google Scholar
  • 104 Lottermoser K, Petras S, Pöge U et al.. The fibrinolytic system in chronic renal failure.  Eur J Med Res. 2001;  6 (9) 372-376
    Search in Google Scholar
  • 105 De Marchi S, Falleti E, Giacomello R et al.. Risk factors for vascular disease and arteriovenous fistula dysfunction in hemodialysis patients.  J Am Soc Nephrol. 1996;  7 (8) 1169-1177
    Search in Google Scholar
  • 106 Inoue A, Wada H, Takagi M et al.. Hemostatic abnormalities in patients with thrombotic complications on maintenance hemodialysis.  Clin Appl Thromb Hemost. 2000;  6 (2) 100-103
    Search in Google Scholar
  • 107 Fan P Y, Schwab S J. Vascular access: concepts for the 1990s.  J Am Soc Nephrol. 1992;  3 (1) 1-11
    Search in Google Scholar
  • 108 Young E W, Dykstra D M, Goodkin D A, Mapes D L, Wolfe R A, Held P J. Hemodialysis vascular access preferences and outcomes in the Dialysis Outcomes and Practice Patterns Study (DOPPS).  Kidney Int. 2002;  61 (6) 2266-2271
    Search in Google Scholar
  • 109 Eleftheriadis T, Antoniadi G, Akritidou A et al.. A case report of recurrent vascular access thrombosis in a hemodialysis patient reveals combined acquired and inherited thrombophilia.  Ther Apher Dial. 2008;  12 (2) 190-192
    Search in Google Scholar
  • 110 Sands J J. Vascular access 2007.  Minerva Urol Nefrol. 2007;  59 (3) 237-249
    Search in Google Scholar
  • 111 Sands J J. Vascular access: the past, present and future.  Blood Purif. 2009;  27 (1) 22-27
    Search in Google Scholar

Martina MontagnanaM.D. 

Sezione di Biochimica Clinica, Università degli Studi di Verona

Ospedale Policlinico G.B. Rossi, P.le Scuro 10, 37134 Verona, Italy

Email: martina.montagnana@med.lu.se