459
Views
3
CrossRef citations to date
0
Altmetric
Review

Endothelial dysfunction and vascular complications after allogeneic hematopoietic cell transplantation: an expert analysis

, , &
Pages 831-840 | Received 10 Jun 2021, Accepted 12 Aug 2021, Published online: 23 Aug 2021

References

  • Passweg JR, Baldomero H, Gratwohl A, et al. The EBMT activity survey: 1990–2010. Bone Marrow Transplant. 2012;47(7):906–923.
  • Majhail NS, Tao L, Bredeson C, et al. Prevalence of hematopoietic cell transplant survivors in the United States. Biol Blood Marrow Transplant. 2013;19(10):1498–1501.
  • Pagliuca S, Michonneau D, Sicre de Fontbrune F, et al. Allogeneic reactivity-mediated endothelial cell complications after HSCT: a plea for consensual definitions. Blood Adv. 2019;3(15):2424–2435.
  • Carreras E, Diaz-Ricart M. The role of the endothelium in the short-term complications of hematopoietic SCT. Bone Marrow Transplant. 2011;46(12):1495–1502.
  • Rondon G, Saliba RM, Chen J, et al. Impact of fluid overload as new toxicity category on hematopoietic stem cell transplantation outcomes. Biol Blood Marrow Transplant. 2017;23(12):2166–2171.
  • Gavriilaki E, Sakellari I, Gavriilaki M, et al. Era in Endothelial Injury Syndromes: toxicity of CAR-T Cells and the Role of Immunity. Int J Mol Sci. 2020;21(11):3886.
  • Gavriilaki E, Brodsky RA. Complementopathies and precision medicine. J Clin Invest. 2020;130(5):2152–2163.
  • Gavriilaki M, Kimiskidis VK, Gavriilaki E. Precision Medicine in Neurology: the Inspirational Paradigm of Complement Therapeutics. Pharmaceuticals (Basel). 2020;13(11):341.
  • Bhatia S, Francisco L, Carter A, et al. Late mortality after allogeneic hematopoietic cell transplantation and functional status of long-term survivors: report from the bone marrow transplant survivor study. Blood. 2007;110(10):3784–3792.
  • Chow EJ, Wong K, Lee SJ, et al. Late cardiovascular complications after hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2014;20(6):794–800.
  • Chow EJ, Mueller BA, Baker KS, et al. Cardiovascular hospitalizations and mortality among recipients of hematopoietic stem cell transplantation. Ann Intern Med. 2011;155(1):21–32.
  • Mouhayar E, Salahudeen A. Hypertension in cancer patients. Texas Heart Institute journal/from the Texas Heart Institute of St. Luke’s Episcopal Hospital, Texas Children’s Hospital. 2011;38(3):263–265.
  • Baker KS, Chow E, Steinberger J. Metabolic syndrome and cardiovascular risk in survivors after hematopoietic cell transplantation. Bone Marrow Transplant. 2012;47(5):619–625.
  • Gavriilaki E, Gkaliagkousi E, Grigoriadis S, et al. Hypertension in hematologic malignancies and hematopoietic cell transplantation: an emerging issue with the introduction of novel treatments. Blood Rev. 2019;35(51):51–58.
  • Baker KS, Ness KK, Weisdorf D, et al. Late effects in survivors of acute leukemia treated with hematopoietic cell transplantation: a report from the bone marrow transplant survivor study. Leukemia. 2010;24(12):2039–2047.
  • Baker KS, Gurney JG, Ness KK, et al. Late effects in survivors of chronic myeloid leukemia treated with hematopoietic cell transplantation: results from the bone marrow transplant survivor study. Blood. 2004;104(6):1898–1906.
  • Rajendran P, Rengarajan T, Thangavel J, et al. The vascular endothelium and human diseases. Int J Biol Sci. 2013;9(10):1057–1069.
  • Shi MM, Kong Y, Song Y, et al. Atorvastatin enhances endothelial cell function in posttransplant poor graft function. Blood. 2016;128(25):2988–2999.
  • Kong Y, Wang Y, Zhang YY, et al. Prophylactic oral NAC reduced poor hematopoietic reconstitution by improving endothelial cells after haploidentical transplantation. Blood Adv. 2019;3(8):1303–1317.
  • Khosla J, Yeh AC, Spitzer TR, et al. Hematopoietic stem cell transplant-associated thrombotic microangiopathy: current paradigm and novel therapies. Bone Marrow Transplant. 2018;53(2):129–137.
  • Harris AC, Young R, Devine S, et al. International, Multicenter Standardization of Acute Graft-versus-Host Disease Clinical Data Collection: a Report from the Mount Sinai Acute GVHD International Consortium. Biol Blood Marrow Transplant. 2016;22(1):4–10.
  • Schoemans HM, Lee SJ, Ferrara JL, et al. EBMT-NIH-CIBMTR Task Force position statement on standardized terminology & guidance for graft-versus-host disease assessment. Bone Marrow Transplant. 2018;53(11):1401–1415.
  • Dalle JH, Giralt SA. Hepatic Veno-Occlusive Disease after Hematopoietic Stem Cell Transplantation: risk Factors and Stratification, Prophylaxis, and Treatment. Biol Blood Marrow Transplant. 2016;22(3):400–409.
  • Mohty M, Malard F, Abecassis M, et al. Revised diagnosis and severity criteria for sinusoidal obstruction syndrome/veno-occlusive disease in adult patients: a new classification from the European society for blood and marrow transplantation. Bone Marrow Transplant. 2016;51(7):906–912.
  • Lewis C, Kim HT, Roeker LE, et al. Incidence, Predictors, and Outcomes of Veno-Occlusive Disease/Sinusoidal Obstruction Syndrome after Reduced-Intensity Allogeneic Hematopoietic Cell Transplantation. Biol Blood Marrow Transplant. 2020;26(3):529–539.
  • Senzolo M, Germani G, Cholongitas E, et al. Veno occlusive disease: update on clinical management. World J Gastroenterol. 2007;13(29):3918–3924.
  • Afessa B, Litzow MR, Tefferi A. Bronchiolitis obliterans and other late onset non-infectious pulmonary complications in hematopoietic stem cell transplantation. Bone Marrow Transplant. 2001;28(5):425–434.
  • Spitzer TR. Engraftment syndrome following hematopoietic stem cell transplantation. Bone Marrow Transplant. 2001;27(9):893–898.
  • Chang L, Frame D, Braun T, et al. Engraftment syndrome after allogeneic hematopoietic cell transplantation predicts poor outcomes. Biol Blood Marrow Transplant. 2014;20(9):1407–1417.
  • Rondon-Clavo C, Scordo M, Hilden P, et al. Early Fluid Overload Is Associated with an Increased Risk of Nonrelapse Mortality after Ex Vivo CD34-Selected Allogeneic Hematopoietic Cell Transplantation. Biol Blood Marrow Transplant. 2018;24(12):2517–2522.
  • Ghimire S, Weber D, Mavin E, et al. Pathophysiology of GvHD and Other HSCT-Related Major Complications. Front Immunol. 2017;8(79). DOI:https://doi.org/10.3389/fimmu.2017.00079
  • Gkaliagkousi E, Gavriilaki E, Vasileiadis I, et al. Endothelial microvesicles circulating in peripheral and coronary circulation are associated with central blood pressure in coronary artery disease. Am J Hypertens. 2019;32(12):1199–1205.
  • Nomura S, Ishii K, Inami N, et al. Evaluation of angiopoietins and cell-derived microparticles after stem cell transplantation. Biol Blood Marrow Transplant. 2008;14(7):766–774.
  • Pihusch V, Rank A, Steber R, et al. Endothelial cell-derived microparticles in allogeneic hematopoietic stem cell recipients. Transplantation. 2006;81(10):1405–1409.
  • Gavriilaki E, Chrysanthopoulou A, Sakellari I, et al. Linking complement activation, coagulation, and neutrophils in transplant-associated thrombotic microangiopathy. Thromb Haemost. 2019;119(9):1433–1440.
  • Gkaliagkousi E, Gavriilaki E, Triantafyllou A, et al. Clinical significance of endothelial dysfunction in essential hypertension. Curr Hypertens Rep. 2015;17(11):85.
  • Sakellari I, Gavriilaki E, Batsis I, et al. Favorable impact of extracorporeal photopheresis in acute and chronic graft versus host disease: prospective single-center study. J Clin Apher. 2018;33(6):654–660.
  • Sakellari I, Gavriilaki E, Kaliou M, et al. Candida is an emerging pathogen beyond the neutropenic period of allogeneic hematopoietic cell transplantation. Clin Transplant. 2017;31(4):e12921.
  • Chatzidimitriou D, Gavriilaki E, Sakellari I, et al. Hematopoietic cell transplantation and emerging viral infections. J Med Virol. 2010;82(3):528–538.
  • Gavriilaki M, Mainou M, Gavriilaki E, et al. Neurologic complications after allogeneic transplantation: a meta-analysis. Ann Clin Transl Neurol. 2019;6(10):2037–2047.
  • Penack O, Marchetti M, Ruutu T, et al. Prophylaxis and management of graft versus host disease after stem-cell transplantation for haematological malignancies: updated consensus recommendations of the European society for blood and marrow transplantation. Lancet Haematol. 2020;7(2):e157–e167.
  • Zeiser R. Immune modulatory effects of statins. Immunology. 2018;154(1):69–75.
  • Magenau JM, Goldstein SC, Peltier D, et al. α1-Antitrypsin infusion for treatment of steroid-resistant acute graft-versus-host disease. Blood. 2018;131(12):1372–1379.
  • Carreras E, Barcelona Endothelium T. Vascular endothelial syndromes after HCT: 2020 update. Bone Marrow Transplant. 2020;55(10):1885–1887.
  • Jodele S, Davies SM, Lane A, et al. Diagnostic and risk criteria for HSCT-associated thrombotic microangiopathy: a study in children and young adults. Blood. 2014;124(4):645–653.
  • Kraft S, Bollinger N, Bodenmann B, et al. High mortality in hematopoietic stem cell transplant-associated thrombotic microangiopathy with and without concomitant acute graft-versus-host disease. Bone Marrow Transplant. 2019;54(4):540–548.
  • Li A, Wu Q, Davis C, et al. Transplant-associated thrombotic microangiopathy is a multifactorial disease unresponsive to immunosuppressant withdrawal. Biol Blood Marrow Transplant. 2019;25(3):570–576.
  • Ye Y, Zheng W, Wang J, et al. Risk and prognostic factors of transplantation-associated thrombotic microangiopathy in allogeneic haematopoietic stem cell transplantation: a nested case control study. Hematol Oncol. 2017;35(4):821–827.
  • Postalcioglu M, Kim HT, Obut F, et al. Impact of thrombotic microangiopathy on renal outcomes and survival after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2018;24(11):2344–2353.
  • Sridharan M, Go RS, Shah MV, et al. Incidence and mortality outcomes in allogeneic transplant-associated thrombotic microangiopathy. Biol Blood Marrow Transplant. 2018;24(3):S329–S330.
  • Zeisbrich M, Becker N, Benner A, et al. Transplant-associated thrombotic microangiopathy is an endothelial complication associated with refractoriness of acute GvHD. Bone Marrow Transplant. 2017;52(10):1399–1405.
  • Jodele S, Dandoy CE, Lane A, et al. Complement blockade for TA-TMA: lessons learned from a large pediatric cohort treated with eculizumab. Blood. 2020;135(13):1049–1057.
  • Dandoy CE, Rotz SR, Alonso PB, et al. Incidence and outcomes of patients with thrombotic microangiopathy after transplant: results of prospective screening through a multi-institutional collaborative. Biol Blood Marrow Transplant. 2020;26(3):S92.
  • Schoettler M, Lehmann LE, Margossian S, et al. Risk factors for transplant-associated thrombotic microangiopathy and mortality in a pediatric cohort. Blood Adv. 2020;4(11):2536–2547.
  • Wall SA, Zhao Q, Yearsley M, et al. Complement-mediated thrombotic microangiopathy as a link between endothelial damage and steroid-refractory GVHD. Blood Adv. 2018;2(20):2619–2628.
  • Sakellari I, Gavriilaki E, Boussiou Z, et al. Transplant-associated thrombotic microangiopathy: an unresolved complication of unrelated allogeneic transplant for hematologic diseases. Hematol Oncol. 2017;35(4):932–934.
  • Dvorak CC, Higham C, Shimano KA. Transplant-Associated Thrombotic Microangiopathy in Pediatric Hematopoietic Cell Transplant Recipients: a Practical Approach to Diagnosis and Management. Front Pediatr. 2019;7(133). DOI:https://doi.org/10.3389/fped.2019.00133
  • Gavriilaki E, Sakellari I, Anagnostopoulos A, et al. Transplant-associated thrombotic microangiopathy: opening Pandora’s box. Bone Marrow Transplant. 2017;52(10):1355–1360.
  • Siami K, Kojouri K, Swisher KK, et al. Thrombotic microangiopathy after allogeneic hematopoietic stem cell transplantation: an autopsy study. Transplantation. 2008;85(1):22–28.
  • Laskin BL, Goebel J, Davies SM, et al. Early clinical indicators of transplant-associated thrombotic microangiopathy in pediatric neuroblastoma patients undergoing auto-SCT. Bone Marrow Transplant. 2011;46(5):682–689.
  • Jodele S. Complement in pathophysiology and treatment of transplant-associated thrombotic microangiopathies. Semin Hematol. 2018;55(3):159–166.
  • Gavriilaki E, Touloumenidou T, Sakellari I, et al. Pretransplant Genetic Susceptibility: clinical Relevance in Transplant-Associated Thrombotic Microangiopathy. Thromb Haemost. 2020;120(4):638–646.
  • Gavriilaki E, Sakellari I, Chatzikonstantinou T, et al. Endothelial and complement activation as predictors of survival in adult allogeneic hematopoietic cell transplantation. Hemasphere. 2021;5(1):e487.
  • Luft T, Benner A, Terzer T, et al. EASIX and mortality after allogeneic stem cell transplantation. Bone Marrow Transplant. 2020;55(3):553–561.
  • Gavriilaki E, Sakellari I, Batsis I, et al. Transplant-associated thrombotic microangiopathy: incidence, prognostic factors, morbidity, and mortality in allogeneic hematopoietic cell transplantation. Clin Transplant. 2018;32(9):e13371.
  • Gavriilaki E, Sakellari I, Bousiou Z, et al. Complement Inhibition with Eculizumab in Adult Transplant-Associated Thrombotic Microangiopathy: opening the Pandora’s Box. Transplantation and Cellular Therapy. 2021;27(3):S270–S271.
  • Gavriilaki E, Sakellari I, Mallouri D, et al. Allogeneic hematopoietic cell transplantation in patients with aplastic anemia and paroxysmal nocturnal hemoglobinuria clones: time for a change. Hemasphere. 2020;4(2):e345.
  • Pan T, Qi J, You T, et al. Circulating Heme Oxygenase-1 and Complement Activation in Transplant-Associated Thrombotic Microangiopathy. Biol Blood Marrow Transplant. 2019;25(8):1486–1491.
  • Rottenstreich A, Hochberg-Klein S, Rund D, et al. The role of N-acetylcysteine in the treatment of thrombotic thrombocytopenic purpura. J Thromb Thrombolysis. 2016;41(4):678–683.
  • Yeates L, Slatter MA, Bonanomi S, et al. Use of defibrotide to treat transplant-associated thrombotic microangiopathy: a retrospective study of the paediatric diseases and inborn errors working parties of the European society of blood and marrow transplantation. Bone Marrow Transplant. 2017;52(5):762–764.
  • Mohty M, Malard F, Abecassis M, et al. Sinusoidal obstruction syndrome/veno-occlusive disease: current situation and perspectives-a position statement from the European Society for Blood and Marrow Transplantation (EBMT). Bone Marrow Transplant. 2015;50(6):781–789.
  • Sakellari I, Batsis I, Bousiou Z, et al. The role of low-dose anti-thymocyte globulin as standard prophylaxis in mismatched and matched unrelated hematopoietic peripheral stem cell transplantation for hematologic malignancies. Clin Lymphoma Myeloma Leuk. 2017;17(10):658–666.
  • Sakellari I, Gavriilaki E, Chatziioannou K, et al. Long-term outcomes of total body irradiation plus cyclophosphamide versus busulfan plus cyclophosphamide as conditioning regimen for acute lymphoblastic leukemia: a comparative study. Ann Hematol. 2018;97(10):1987–1994.
  • Lambert J, Pautas C, Terre C, et al. Gemtuzumab ozogamicin for de novo acute myeloid leukemia: final efficacy and safety updates from the open-label, phase 3 ALFA-0701 trial. Haematologica. 2018;
  • Jabbour EJ, DeAngelo DJ, Stelljes M, et al. Efficacy and safety analysis by age cohort of inotuzumab ozogamicin in patients with relapsed or refractory acute lymphoblastic leukemia enrolled in INO-VATE. Cancer. 2018;124(8):1722–1732.
  • Batsis I, Yannaki E, Kaloyannidis P, et al. Veno-occlusive disease prophylaxis with fresh frozen plasma and heparin in bone marrow transplantation. Thromb Res. 2006;118(5):611–618.
  • Corbacioglu S, Carreras E, Ansari M, et al. Diagnosis and severity criteria for sinusoidal obstruction syndrome/veno-occlusive disease in pediatric patients: a new classification from the European society for blood and marrow transplantation. Bone Marrow Transplant. 2018;53(2):138–145.
  • De Ledinghen V, Villate A, Robin M, et al. Sinusoidal obstruction syndrome. Clin Res Hepatol Gastroenterol. 2020;44(4):480–485.
  • Ruutu T, Juvonen E, Remberger M, et al. Improved survival with ursodeoxycholic acid prophylaxis in allogeneic stem cell transplantation: long-term follow-up of a randomized study. Biol Blood Marrow Transplant. 2014;20(1):135–138.
  • Kebriaei P, Cutler C, De Lima M, et al. Management of important adverse events associated with inotuzumab ozogamicin: expert panel review. Bone Marrow Transplant. 2018;53(4):449–456.
  • Faraci M, Bertaina A, Luksch R, et al. Sinusoidal Obstruction Syndrome/Veno-Occlusive Disease after Autologous or Allogeneic Hematopoietic Stem Cell Transplantation in Children: a retrospective study of the Italian Hematology-Oncology Association-Hematopoietic Stem Cell Transplantation Group. Biol Blood Marrow Transplant. 2019;25(2):313–320.
  • Lee AC, Aung L. Treatment of hepatic veno-occlusive disease in children with N-acetylcysteine. Pediatr Blood Cancer. 2019;66(2):e27518.
  • Dignan FL, Wynn RF, Hadzic N, et al. BCSH/BSBMT guideline: diagnosis and management of veno-occlusive disease (sinusoidal obstruction syndrome) following haematopoietic stem cell transplantation. Br J Haematol. 2013;163(4):444–457.
  • Smith FO, Johnson MS, Scherer LR, et al. Transjugular intrahepatic portosystemic shunting (TIPS) for treatment of severe hepatic veno-occlusive disease. Bone Marrow Transplant. 1996;18(3):643–646.
  • Hildebrandt GC, Chao N. Endothelial cell function and endothelial-related disorders following haematopoietic cell transplantation. Br J Haematol. 2020;190(4):508–519.
  • Afessa B, Tefferi A, Litzow MR, et al. Diffuse alveolar hemorrhage in hematopoietic stem cell transplant recipients. Am J Respir Crit Care Med. 2002;166(5):641–645.
  • Spitzer TR. Engraftment syndrome: double-edged sword of hematopoietic cell transplants. Bone Marrow Transplant. 2015;50(4):469–475.
  • Lucchini G, Willasch AM, Daniel J, et al. Epidemiology, risk factors, and prognosis of capillary leak syndrome in pediatric recipients of stem cell transplants: a retrospective single-center cohort study. Pediatr Transplant. 2016;20(8):1132–1136.
  • Armenian SH, Chemaitilly W, Chen M, et al. National institutes of health hematopoietic cell transplantation late effects initiative: the cardiovascular disease and associated risk factors working group report. Biol Blood Marrow Transplant. 2017;23(2):201–210.
  • Whelton PK, Carey RM, Aronow WS, et al. 2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA Guideline for the Prevention, Detection, Evaluation, and Management of High Blood Pressure in Adults: executive Summary: a Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Circulation. 2018;138(17):e426–e483.
  • Sureddi RK, Amani F, Hebbar P, et al. Atrial fibrillation following autologous stem cell transplantation in patients with multiple myeloma: incidence and risk factors. Ther Adv Cardiovasc Dis. 2012;6(6):229–236.
  • Steuter JA, Villanueva ML, Loberiza FR, et al. Factors affecting the development of atrial fibrillation and atrial flutter (AF/AFL) following autologous hematopoietic SCT (auto-HSCT). Bone Marrow Transplant. 2013;48(7):963–965.
  • Fatema K, Gertz MA, Barnes ME, et al. Acute weight gain and diastolic dysfunction as a potent risk complex for post stem cell transplant atrial fibrillation. Am J Hematol. 2009;84(8):499–503.
  • Tichelli A, Bucher C, Rovo A, et al. Premature cardiovascular disease after allogeneic hematopoietic stem-cell transplantation. Blood. 2007;110(9):3463–3471.
  • Anderson KM, Odell PM, Wilson PW, et al. Cardiovascular disease risk profiles. Am Heart J. 1991;121(1):293–298.
  • Anderson KM, Wilson PW, Odell PM, et al. An updated coronary risk profile. A statement for health professionals. Circulation. 1991;83(1):356–362.
  • Wilson PW, D’Agostino RB, Levy D, et al. Prediction of coronary heart disease using risk factor categories. Circulation. 1998;97(18):1837–1847.
  • Conroy RM, Pyorala K, Fitzgerald AP, et al. Estimation of ten-year risk of fatal cardiovascular disease in Europe: the SCORE project. Eur Heart J. 2003;24(11):987–1003.
  • Hippisley-Cox J, Coupland C, Robson J, et al. Derivation, validation, and evaluation of a new QRISK model to estimate lifetime risk of cardiovascular disease: cohort study using QResearch database. BMJ. 2010;341(dec09 1):c6624.
  • Hippisley-Cox J, Coupland C, Vinogradova Y, et al. Performance of the QRISK cardiovascular risk prediction algorithm in an independent UK sample of patients from general practice: a validation study. Heart. 2008;94(1):34–39.
  • Hippisley-Cox J, Coupland C, Vinogradova Y, et al. Derivation and validation of QRISK, a new cardiovascular disease risk score for the United Kingdom: prospective open cohort study. BMJ. 2007;335(7611):136.
  • Williams B, Mancia G, Spiering W, et al. ESC/ESH Guidelines for the management of arterial hypertension. Eur Heart J. 2018;39(33):3021–3104.
  • Goff DC Jr., Lloyd-Jones DM, Bennett G, et al. ACC/AHA guideline on the assessment of cardiovascular risk: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014;63(25):2935–2959.
  • Damen JA, Hooft L, Schuit E, et al. Prediction models for cardiovascular disease risk in the general population: systematic review. BMJ. 2016;353:i2416.
  • Majhail NS, Flowers ME, Ness KK, et al. High prevalence of metabolic syndrome after allogeneic hematopoietic cell transplantation. Bone Marrow Transplant. 2009;43(1):49–54.
  • Tichelli A, Passweg J, Wojcik D, et al. Late cardiovascular events after allogeneic hematopoietic stem cell transplantation: a retrospective multicenter study of the late effects working party of the European group for blood and marrow transplantation. Haematologica. 2008;93(8):1203–1210.
  • Pophali PA, Klotz JK, Ito S, et al. Male survivors of allogeneic hematopoietic stem cell transplantation have a long term persisting risk of cardiovascular events. Exp Hematol. 2014;42(2):83–89.
  • Khalil MMI, Lipton JH, Atenafu EG, et al. Impact of comorbidities constituting the hematopoietic cell transplant (HCT)-comorbidity index on the outcome of patients undergoing allogeneic HCT for acute myeloid leukemia. Eur J Haematol. 2018;100(2):198–205.
  • Bejar MT, Hernandez-Vera R, Vilahur G, et al. Bone marrow cell transplant from donors with cardiovascular risk factors increases the pro-atherosclerotic phenotype in the recipients. Am J Transplant. 2016;16(12):3392–3403.
  • Crowson CS, Gabriel SE, Semb AG, et al. Rheumatoid arthritis-specific cardiovascular risk scores are not superior to general risk scores: a validation analysis of patients from seven countries. Rheumatology (Oxford). 2017;56(7):1102–1110.
  • Armenian SH, Yang D, Teh JB, et al. Prediction of cardiovascular disease among hematopoietic cell transplantation survivors. Blood Adv. 2018;2(14):1756–1764.
  • Triantafyllou A, Anyfanti P, Zabulis X, et al. Accumulation of microvascular target organ damage in newly diagnosed hypertensive patients. J Am Soc Hypertens. 2014;8(8):542–549.
  • Dipla K, Triantafyllou A, Grigoriadou I, et al. Impairments in microvascular function and skeletal muscle oxygenation in women with gestational diabetes mellitus: links to cardiovascular disease risk factors. Diabetologia. 2017;60(1):192–201.
  • Mahe G, Humeau-Heurtier A, Durand S, et al. Assessment of skin microvascular function and dysfunction with laser speckle contrast imaging. Circ Cardiovasc Imaging. 2012;5(1):155–163.
  • Roustit M, Cracowski JL. Assessment of endothelial and neurovascular function in human skin microcirculation. Trends Pharmacol Sci. 2013;34(7):373–384.
  • Humeau-Heurtier A, Abraham P, Mahe G. Analysis of laser speckle contrast images variability using a novel empirical mode decomposition: comparison of results with laser Doppler flowmetry signals variability. IEEE Trans Med Imaging. 2015;34(2):618–627.
  • Gavriilaki E, Sakellari I, Anyfanti P, et al. Assessment of endothelial injury and pro-coagulant activity using circulating microvesicles in survivors of allogeneic hematopoietic cell transplantation. Int J Mol Sci. 2020;21(24):9768.
  • Jernberg T, Hasvold P, Henriksson M, et al. Cardiovascular risk in post-myocardial infarction patients: nationwide real world data demonstrate the importance of a long-term perspective. Eur Heart J. 2015;36(19):1163–1170.
  • Stavrou EX. Thromboinflammatory effects of RBC microvesicles. Blood. 2020;135(10):708–709.
  • Gavriilaki E, Gkaliagkousi E, Sakellari I, et al. Early Prediction of Cardiovascular Risk after Hematopoietic Cell Transplantation: are We There Yet? Biol Blood Marrow Transplant. 2019;25(10):e310–e316.
  • Lia G, Brunello L, Bruno S, et al. Extracellular vesicles as potential biomarkers of acute graft-vs-host disease. Leukemia. 2018;32(3):765–773.
  • Gkaliagkousi E, Gavriilaki E, Doumas M, et al. Cardiovascular risk in rheumatoid arthritis: pathogenesis, diagnosis, and management. J Clin Rheumatol. 2012;18(8):422–430.
  • Borchert-Morlins B, Memaran N, Sauer M, et al. Cardiovascular risk factors and subclinical organ damage after hematopoietic stem cell transplantation in pediatric age. Bone Marrow Transplant. 2018;53(8):983–992.
  • Espino G, Denney J, Furlong T, et al. Assessment of myocardial hypertrophy by echocardiography in adult patients receiving tacrolimus or cyclosporine therapy for prevention of acute GVHD. Bone Marrow Transplant. 2001;28(12):1097–1103.
  • Dogan A, Dogdu O, Ozdogru I, et al. Cardiac effects of chronic graft-versus-host disease after stem cell transplantation. Texas Heart Institute journal/from the Texas Heart Institute of St. Luke’s Episcopal Hospital, Texas Children’s Hospital. 2013;40(4):428–434.
  • Kupari M, Volin L, Suokas A, et al. Cardiac involvement in bone marrow transplantation: electrocardiographic changes, arrhythmias, heart failure and autopsy findings. Bone Marrow Transplant. 1990;5(2):91–98.
  • Sakellari I, Barbouti A, Bamichas G, et al. GVHD-associated chronic kidney disease after allogeneic haematopoietic cell transplantation. Bone Marrow Transplant. 2013;48(10):1329–1334.
  • Socie G, Mary JY, Esperou H, et al. Health and functional status of adult recipients 1 year after allogeneic haematopoietic stem cell transplantation. Br J Haematol. 2001;113(1):194–201.
  • Hingorani S, Finn LS, Pao E, et al. Urinary elafin and kidney injury in hematopoietic cell transplant recipients. Clin J Am Soc Nephrol. 2015;10(1):12–20.
  • Avolio AP, Chen SG, Wang RP, et al. Effects of aging on changing arterial compliance and left ventricular load in a northern Chinese urban community. Circulation. 1983;68(1):50–58.
  • Avolio AP, Deng FQ, Li WQ, et al. Effects of aging on arterial distensibility in populations with high and low prevalence of hypertension: comparison between urban and rural communities in China. Circulation. 1985;71(2):202–210.
  • Gkaliagkousi E, Anyfanti P, Triantafyllou A, et al. Aldosterone as a mediator of microvascular and macrovascular damage in a population of normotensive to early-stage hypertensive individuals. J Am Soc Hypertens. 2018;12(1):50–57.
  • Gkaliagkousi E, Douma S. The pathogenesis of arterial stiffness and its prognostic value in essential hypertension and cardiovascular diseases. Hippokratia. 2009;13(2):70–75.
  • Vlachopoulos C, Aznaouridis K, O’Rourke MF, et al. Prediction of cardiovascular events and all-cause mortality with central haemodynamics: a systematic review and meta-analysis. Eur Heart J. 2010;31(15):1865–1871.
  • Vlachopoulos C, Aznaouridis K, Stefanadis C. Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol. 2010;55(13):1318–1327.
  • Anyfanti P, Triantafyllou A, Gkaliagkousi E, et al. Association of non-invasive hemodynamics with arterial stiffness in rheumatoid arthritis. Scand Cardiovasc J. 2018;52(4):171–176.
  • Anyfanti P, Triantafyllou A, Chatzimichailidou S, et al. Arterial stiffness indexes and serum cytokine levels in seronegative spondyloarthritis: relationships between stiffness markers and metabolic and immunoinflammatory variables: comments on the article by Tuttolomondo et al. Scand J Rheumatol. 2016;45(6):539–540.
  • Paiman EHM, Louwerens M, Bresters D, et al. Late effects of pediatric hematopoietic stem cell transplantation on left ventricular function, aortic stiffness and myocardial tissue characteristics. J Cardiovasc Magn Reson. 2019;21(1):6.
  • Vatanen A, Sarkola T, Ojala TH, et al. Radiotherapy-related arterial intima thickening and plaque formation in childhood cancer survivors detected with very-high resolution ultrasound during young adulthood. Pediatr Blood Cancer. 2015;62(11):2000–2006.
  • Dengel DR, Kelly AS, Zhang L, et al. Vascular Structure and Function in Cancer Survivors after Hematopoietic Stem Cell Transplantation. Biol Blood Marrow Transplant. 2019;25(1):151–156.
  • Bots ML, Grobbee DE. Intima media thickness as a surrogate marker for generalised atherosclerosis. Cardiovasc Drugs Ther. 2002;16(4):341–351.
  • van Popele NM, Grobbee DE, Bots ML, et al. Association between arterial stiffness and atherosclerosis: the Rotterdam Study. Stroke. 2001;32(2):454–460.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.