Clinical and Experimental Pediatrics

대한소아청소년과학회 (The Korean Pediatric Society)
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The use of extracorporeal membrane oxygenation in children with acute fulminant myocarditis

  • Heinsar, Silver (Critical Care Research Group, Faculty of Medicine, University of Queensland and The Prince Charles Hospital) ;
  • Raman, Sainath (Critical Care Research Group, Faculty of Medicine, University of Queensland and The Prince Charles Hospital) ;
  • Suen, Jacky Y. (Critical Care Research Group, Faculty of Medicine, University of Queensland and The Prince Charles Hospital) ;
  • Cho, Hwa Jin (Critical Care Research Group, Faculty of Medicine, University of Queensland and The Prince Charles Hospital) ;
  • Fraser, John F. (Critical Care Research Group, Faculty of Medicine, University of Queensland and The Prince Charles Hospital)
  • 투고 : 2020.05.04
  • 심사 : 2020.07.02
  • 발행 : 2021.05.15
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초록

Acute fulminant myocarditis (AFM) occurs as an inflammatory response to an initial myocardial insult. Its rapid and deadly progression calls for prompt diagnosis with aggressive treatment measures. The demonstration of its excellent recovery potential has led to increasing use of mechanical circulatory support, especially extracorporeal membrane oxygenation (ECMO). Arrhythmias, organ failure, elevated cardiac biomarkers, and decreased ventricular function at presentation predict requirement for ECMO. In these patients, ECMO should be considered earlier as the clinical course of AFM can be unpredictable and can lead to rapid haemodynamic collapse. Key uncertainties that clinicians face when managing children with AFM such as timing of initiation of ECMO and left ventricular decompression need further investigation.

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과제정보

Hwa Jin Cho acknowledges the support of a grant NRF-2018R1D1A1A02085975 from National Research Foundation of Korea and a grant BCRI18028 from the Chonnam National University Hospital Biomedical Research Institute. Silver Heinsar received a PhD Scholarship from The Prince Charles Hospital Foundation. Authors acknowledge Sarfaraz Rahiman and In Seok Jeong for reviewing the paper before the submission and Dr. Samia Farah, MD for the illustration, which was created with BioRender.com.

참고문헌

  1. Magnani JW, Dec GW. Myocarditis. Circulation 2006;113:876-90. https://doi.org/10.1161/CIRCULATIONAHA.105.584532
  2. Extracorporeal Life Support Organization. ECLS Registry Report. International Summary 2020 January.
  3. Mounts AW, Amr S, Jamshidi R, Groves C, Dwyer D, Guarner J, et al. A cluster of fulminant myocarditis cases in children, Baltimore, Maryland, 1997. Pediatr Cardiol 2001;22:34-9. https://doi.org/10.1007/s002460010148
  4. Amabile N, Fraisse A, Bouvenot J, Chetaille P, Ovaert C. Outcome of acute fulminant myocarditis in children. Heart 2006;92:1269-73. https://doi.org/10.1136/hrt.2005.078402
  5. Sankar J, Khalil S, Jeeva Sankar M, Kumar D, Dubey N. Short-term outcomes of acute fulminant myocarditis in children. Pediatr Cardiol 2011;32:885-90. https://doi.org/10.1007/s00246-011-0007-8
  6. Forcada P, Beigelman R, Milei J. Inapparent myocarditis and sudden death in pediatrics. Diagnosis by immunohistochemical staining. Int J Cardiol 1996;56:93-7. https://doi.org/10.1016/0167-5273(96)02752-0
  7. Weber MA, Ashworth MT, Risdon RA, Malone M, Burch M, Sebire NJ. Clinicopathological features of paediatric deaths due to myocarditis: an autopsy series. Arch Dis Child 2008;93:594-8. https://doi.org/10.1136/adc.2007.128686
  8. Doolan A, Langlois N, Semsarian C. Causes of sudden cardiac death in young Australians. Med J Aust 2004;180:110-2. https://doi.org/10.5694/j.1326-5377.2004.tb05830.x
  9. deSa DJ. Isolated myocarditis as a cause of sudden death in the first year of life. Forensic Sci Int 1986;30:113-7. https://doi.org/10.1016/0379-0738(86)90005-8
  10. Rasten-Almqvist P, Eksborg S, Rajs J. Myocarditis and sudden infant death syndrome. Apmis 2002;110:469-80. https://doi.org/10.1034/j.1600-0463.2002.100605.x
  11. Shimizu C, Rambaud C, Cheron G, Rouzioux C, Lozinski GM, Rao A, et al. Molecular identification of viruses in sudden infant death associated with myocarditis and pericarditis. Pediatr Infect Dis J 1995;14:584-8. https://doi.org/10.1097/00006454-199507000-00006
  12. Dettmeyer R, Baasner A, Schlamann M, Haag C, Madea B. Coxsackie B3 myocarditis in 4 cases of suspected sudden infant death syndrome: diagnosis by immunohistochemical and molecular-pathologic investigations. Pathol Res Pract 2002;198:689-96. https://doi.org/10.1078/0344-0338-00322
  13. Matsuura H, Ichida F, Saji T, Ogawa S, Waki K, Kaneko M, et al. Clinical features of acute and fulminant myocarditis in children - 2nd Nationwide Survey by Japanese Society of Pediatric Cardiology and Cardiac Surgery. Circ J 2016;80:2362-8. https://doi.org/10.1253/circj.CJ-16-0234
  14. Ghelani SJ, Spaeder MC, Pastor W, Spurney CF, Klugman D. Demographics, trends, and outcomes in pediatric acute myocarditis in the United States, 2006 to 2011. Circ Cardiovasc Qual Outcomes 2012;5:622-7. https://doi.org/10.1161/CIRCOUTCOMES.112.965749
  15. Lyden DC, Olszewski J, Feran M, Job LP, Huber SA. Coxsackievirus B-3-induced myocarditis. Effect of sex steroids on viremia and infectivity of cardiocytes. Am J Pathol 1987;126:432-8.
  16. utts RJ, Boyle GJ, Deshpande SR, Gambetta K, Knecht KR, Prada-Ruiz CA, et al. Characteristics of clinically diagnosed pediatric myocarditis in a contemporary multi-center cohort. Pediatr Cardiol 2017;38:1175-82. https://doi.org/10.1007/s00246-017-1638-1
  17. Canter CE, Simpson KE. Diagnosis and treatment of myocarditis in children in the current era. Circulation 2014;129:115-28. https://doi.org/10.1161/CIRCULATIONAHA.113.001372
  18. Olinde KD, O'Connell JB. Inflammatory heart disease: pathogenesis, clinical manifestations, and treatment of myocarditis. Annu Rev Med 1994;45:481-90. https://doi.org/10.1146/annurev.med.45.1.481
  19. Klugman D, Berger JT, Sable CA, He J, Khandelwal SG, Slonim AD. Pediatric patients hospitalized with myocarditis: a multi-institutional analysis. Pediatr Cardiol 2010;31:222-8. https://doi.org/10.1007/s00246-009-9589-9
  20. Isogai T, Yasunaga H, Matsui H, Tanaka H, Horiguchi H, Fushimi K. Effect of intravenous immunoglobulin for fulminant myocarditis on in-hospital mortality: propensity score analyses. J Card Fail 2015;21:391-7. https://doi.org/10.1016/j.cardfail.2015.01.004
  21. Li Y, Yu Y, Chen S, Liao Y, Du J. Corticosteroids and intravenous immunoglobulin in pediatric myocarditis: a meta-analysis. Front Pediatr 2019;7:342. https://doi.org/10.3389/fped.2019.00342
  22. Bejiqi R, Retkoceri R, Maloku A, Mustafa A, Bejiqi H, Bejiqi R. The diagnostic and clinical approach to pediatric myocarditis: a review of the current literature. Open Access Maced J Med Sci 2019;7:162-73. https://doi.org/10.3889/oamjms.2019.010
  23. Casadonte JR, Mazwi ML, Gambetta KE, Palac HL, McBride ME, Eltayeb OM, et al. Risk factors for cardiac arrest or mechanical circulatory support in children with fulminant myocarditis. Pediatr Cardiol 2017;38:128-34. https://doi.org/10.1007/s00246-016-1493-5
  24. Chang YJ, Hsiao HJ, Hsia SH, Lin JJ, Hwang MS, Chung HT, et al. Analysis of clinical parameters and echocardiography as predictors of fatal pediatric myocarditis. PLoS One 2019;14:e0214087. https://doi.org/10.1371/journal.pone.0214087
  25. Inaba O, Satoh Y, Isobe M, Yamamoto T, Nagao K, Takayama M. Factors and values at admission that predict a fulminant course of acute myocarditis: data from Tokyo CCU network database. Heart Vessels 2017;32:952-9. https://doi.org/10.1007/s00380-017-0960-0
  26. Schubert S, Opgen-Rhein B, Boehne M, Weigelt A, Wagner R, Muller G, et al. Severe heart failure and the need for mechanical circulatory support and heart transplantation in pediatric patients with myocarditis: Results from the prospective multicenter registry "MYKKE". Pediatr Transplant 2019;23:e13548.
  27. Yang F, Wang J, Li W, Xu Y, Wan K, Zeng R, et al. The prognostic value of late gadolinium enhancement in myocarditis and clinically suspected myocarditis: systematic review and meta-analysis. Eur Radiol 2020;30:2616-26. https://doi.org/10.1007/s00330-019-06643-5
  28. Hsu KH, Chi NH, Yu HY, Wang CH, Huang SC, Wang SS, et al. Extracorporeal membranous oxygenation support for acute fulminant myocarditis: analysis of a single center's experience. Eur J Cardiothorac Surg 2011;40:682-8.
  29. Lin KM, Li MH, Hsieh KS, Kuo HC, Cheng MC, Sheu JJ, et al. Impact of extracorporeal membrane oxygenation on acute fulminant myocarditis-related hemodynamic compromise arrhythmia in children. Pediatr Neonatol 2016;57:480-7. https://doi.org/10.1016/j.pedneo.2016.02.002
  30. Nahum E, Dagan O, Lev A, Shukrun G, Amir G, Frenkel G, et al. Favorable outcome of pediatric fulminant myocarditis supported by extracorporeal membranous oxygenation. Pediatr Cardiol 2010;31:1059-63. https://doi.org/10.1007/s00246-010-9765-y
  31. Wu HP, Lin MJ, Yang WC, Wu KH, Chen CY. Predictors of extracorporeal membrane oxygenation support for children with acute myocarditis. Biomed Res Int 2017;2017:2510695.
  32. Kurkluoglu M, Hynes CF, Alfares FA, El-Sayed Ahmed MM, Peer SM, Zurakowski D, et al. Choice of peripheral venoarterial extra-corporeal membrane oxygenation cannulation site in patients above 15 kilograms. J Card Surg 2015;30:461-5. https://doi.org/10.1111/jocs.12538
  33. Gander JW, Fisher JC, Reichstein AR, Gross ER, Aspelund G, Middles-worth W, et al. Limb ischemia after common femoral artery cannulation for venoarterial extracorporeal membrane oxygenation: an unresolved problem. J Pediatr Surg 2010;45:2136-40. https://doi.org/10.1016/j.jpedsurg.2010.07.005
  34. Butt W, Heard M, Peek GJ. Clinical management of the extracorporeal membrane oxygenation circuit. Pediatr Crit Care Med 2013;14(5 Suppl 1):S13-9. https://doi.org/10.1097/PCC.0b013e318292ddc8
  35. Ostadal P, Mlcek M, Kruger A, Hala P, Lacko S, Mates M, et al. Increasing venoarterial extracorporeal membrane oxygenation flow negatively affects left ventricular performance in a porcine model of cardiogenic shock. J Transl Med 2015;13:266. https://doi.org/10.1186/s12967-015-0634-6
  36. Van Linthout S, Tschope C. Inflammation - cause or consequence of heart failure or both? Curr Heart Fail Rep 2017;14:251-65. https://doi.org/10.1007/s11897-017-0337-9
  37. Jung SY, Shin HJ, Jung JW, Park HK, Shin YR, Park YH, et al. Extracorporeal life support can be a first-line treatment in children with acute fulminant myocarditis. Interact Cardiovasc Thorac Surg 2016;23:24752.
  38. Kotani Y, Chetan D, Rodrigues W, Sivarajan VB, Gruenwald C, Guerguerian AM, et al. Left atrial decompression during venoarterial extracorporeal membrane oxygenation for left ventricular failure in children: current strategy and clinical outcomes. Artif Organs 2013;37:29-36. https://doi.org/10.1111/j.1525-1594.2012.01534.x
  39. Lin YJ, Liu HY, Kuo HC, Huang CF, Hsu MH, Cheng MC, et al. Left ventricle decompression strategies in pediatric peripheral extracorporeal membrane oxygenation. Acta Cardiol Sin 2019;35:335-41.
  40. Rajagopal SK, Almond CS, Laussen PC, Rycus PT, Wypij D, Thiagarajan RR. Extracorporeal membrane oxygenation for the support of infants, children, and young adults with acute myocarditis: a review of the Extracorporeal Life Support Organization registry. Crit Care Med 2010;38:382-7. https://doi.org/10.1097/CCM.0b013e3181bc8293
  41. Eastaugh LJ, Thiagarajan RR, Darst JR, McElhinney DB, Lock JE, Marshall AC. Percutaneous left atrial decompression in patients supported with extracorporeal membrane oxygenation for cardiac disease. Pediatr Crit Care Med 2015;16:59-65. https://doi.org/10.1097/PCC.0000000000000276
  42. Russo JJ, Aleksova N, Pitcher I, Couture E, Parlow S, Faraz M, et al. Left ventricular unloading during extracorporeal membrane oxygenation in patients with cardiogenic shock. J Am Coll Cardiol 2019;73:654-62 https://doi.org/10.1016/S0735-1097(19)31262-8
  43. Dalton HJ, Reeder R, Garcia-Filion P, Holubkov R, Berg RA, Zuppa A, et al. Factors associated with bleeding and thrombosis in children receiving extracorporeal membrane oxygenation. Am J Respir Crit Care Med 2017;196:762-71. https://doi.org/10.1164/rccm.201609-1945oc
  44. Millar JE, Fanning JP, McDonald CI, McAuley DF, Fraser JF. The inflammatory response to extracorporeal membrane oxygenation (ECMO): a review of the pathophysiology. Crit Care 2016;20:387. https://doi.org/10.1186/s13054-016-1570-4
  45. Monagle P, Chan A, Massicotte P, Chalmers E, Michelson AD. Antithrombotic therapy in children: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest 2004;126(3 Suppl):645S-687S. https://doi.org/10.1378/chest.126.3_suppl.645S
  46. Barton R, Ignjatovic V, Monagle P. Anticoagulation during ECMO in neonatal and paediatric patients. Thromb Res 2019;173:172-7. https://doi.org/10.1016/j.thromres.2018.05.009
  47. Monagle P, Newall F, Campbell J. Anticoagulation in neonates and children: pitfalls and dilemmas. Blood Rev 2010;24:151-62. https://doi.org/10.1016/j.blre.2010.06.003
  48. O'Meara LC, Alten JA, Goldberg KG, Timpa JG, Phillips J, Laney D, et al. Anti-xa directed protocol for anticoagulation management in children supported with extracorporeal membrane oxygenation. ASAIO J 2015;61:339-44. https://doi.org/10.1097/MAT.0000000000000204
  49. Ignjatovic V, Summerhayes R, Than J, Gan A, Monagle P. Therapeutic range for unfractionated heparin therapy: age-related differences in response in children. J Thromb Haemost 2006;4:2280-2. https://doi.org/10.1111/j.1538-7836.2006.02136.x
  50. Monagle P, Barnes C, Ignjatovic V, Furmedge J, Newall F, Chan A, et al. Developmental haemostasis. Impact for clinical haemostasis laboratories. Thromb Haemost 2006;95:362-72. https://doi.org/10.1267/THRO06020362
  51. Cho HJ, Kim DW, Kim GS, Jeong IS. Anticoagulation therapy during extracorporeal membrane oxygenator support in pediatric patients. Chonnam Med J 2017;53:110-7. https://doi.org/10.4068/cmj.2017.53.2.110
  52. Pieri M, Agracheva N, Bonaveglio E, Greco T, De Bonis M, Covello RD, et al. Bivalirudin versus heparin as an anticoagulant during extracorporeal membrane oxygenation: a case-control study. J Cardiothorac Vasc Anesth 2013;27:30-4. https://doi.org/10.1053/j.jvca.2012.07.019
  53. Bembea MM, Annich G, Rycus P, Oldenburg G, Berkowitz I, Pronovost P. Variability in anticoagulation management of patients on extracorporeal membrane oxygenation: an international survey. Pediatr Crit Care Med 2013;14:e77-84. https://doi.org/10.1097/PCC.0b013e31827127e4
  54. Liveris A, Bello RA, Friedmann P, Duffy MA, Manwani D, Killinger JS, et al. Anti-factor Xa assay is a superior correlate of heparin dose than activated partial thromboplastin time or activated clotting time in pediatric extracorporeal membrane oxygenation*. Pediatr Crit Care Med 2014;15:e72-9. https://doi.org/10.1097/PCC.0000000000000028
  55. Northrop MS, Sidonio RF, Phillips SE, Smith AH, Daphne HC, Pietsch JB, et al. The use of an extracorporeal membrane oxygenation anticoagulation laboratory protocol is associated with decreased blood product use, decreased hemorrhagic complications, and increased circuit life. Pediatr Crit Care Med 2015;16:66-74. https://doi.org/10.1097/PCC.0000000000000278
  56. Hervey-Jumper SL, Annich GM, Yancon AR, Garton HJ, Muraszko KM, Maher CO. Neurological complications of extracorporeal membrane oxygenation in children. J Neurosurg Pediatr 2011;7:338-44. https://doi.org/10.3171/2011.1.PEDS10443
  57. Hardart GE, Fackler JC. Predictors of intracranial hemorrhage during neonatal extracorporeal membrane oxygenation. J Pediatr 1999;134:156-9. https://doi.org/10.1016/S0022-3476(99)70408-7
  58. Teele SA, Allan CK, Laussen PC, Newburger JW, Gauvreau K, Thiagarajan RR. Management and outcomes in pediatric patients presenting with acute fulminant myocarditis. J Pediatr 2011;158:638-43.e1. https://doi.org/10.1016/j.jpeds.2010.10.015
  59. Cho SM, Farrokh S, Whitman G, Bleck TP, Geocadin RG. Neurocritical care for extracorporeal membrane oxygenation patients. Crit Care Med 2019;47:1773-81. https://doi.org/10.1097/ccm.0000000000004060
  60. Werho DK, Pasquali SK, Yu S, Donohue J, Annich GM, Thiagarajan RR, et al. Hemorrhagic complications in pediatric cardiac patients on extracorporeal membrane oxygenation: an analysis of the Extracorporeal Life Support Organization Registry. Pediatr Crit Care Med 2015;16:276-88. https://doi.org/10.1097/PCC.0000000000000345
  61. Said AS, Guilliams KP, Bembea MM. Neurological monitoring and complications of pediatric extracorporeal membrane oxygenation support. Pediatr Neurol 2020;108:31-9. https://doi.org/10.1016/j.pediatrneurol.2020.03.014
  62. Extracorporeal Life Support Organization. Guidelines for Pediatric Cardiac Failure [Internet]. Ann Arbor (MI): Extracorporeal Life Support Organization; [cited 2020 15 Jan]. Available from: http://www.elso.org/resources/guidelines.aspx.
  63. Aissaoui N, Luyt CE, Leprince P, Trouillet JL, Leger P, Pavie A, et al. Predictors of successful extracorporeal membrane oxygenation (ECMO) weaning after assistance for refractory cardiogenic shock. Intensive Care Med 2011;37:1738-45. https://doi.org/10.1007/s00134-011-2358-2
  64. Duncan BW, Bohn DJ, Atz AM, French JW, Laussen PC, Wessel DL. Mechanical circulatory support for the treatment of children with acute fulminant myocarditis. J Thorac Cardiovasc Surg 2001;122:440-8. https://doi.org/10.1067/mtc.2001.115243
  65. Foerster SR, Canter CE, Cinar A, Sleeper LA, Webber SA, Pahl E, et al. Ventricular remodeling and survival are more favorable for myocarditis than for idiopathic dilated cardiomyopathy in childhood: an outcomes study from the Pediatric Cardiomyopathy Registry. Circ Heart Fail 2010;3:689-97. https://doi.org/10.1161/CIRCHEARTFAILURE.109.902833
  66. Morales DLS, Rossano JW, VanderPluym C, Lorts A, Cantor R, St Louis JD, et al. Third Annual Pediatric Interagency Registry for Mechanical Circulatory Support (Pedimacs) report: preimplant characteristics and outcomes. Ann Thorac Surg 2019;107:993-1004. https://doi.org/10.1016/j.athoracsur.2019.01.038
  67. Yoshioka D, Takeda K, Takayama H, Naka Y. Low INTERMACS profiles: one-stage durable LVAD implantation for INTERMACS level 1: indications and contraindications. In: Montalto A, Loforte A, Musumeci F, Krabatsch T, Slaughter MS, editors. Mechanical circulatory support in end-stage heart failure: a practical manual. Cham: Springer International Publishing; 2017:115-9.
  68. McCarthy RE 3rd, Boehmer JP, Hruban RH, Hutchins GM, Kasper EK, Hare JM, et al. Long-term outcome of fulminant myocarditis as compared with acute (nonfulminant) myocarditis. N Engl J Med 2000;342:690-5. https://doi.org/10.1056/NEJM200003093421003
  69. Boyle K, Felling R, Yiu A, Battarjee W, Schwartz JM, Salorio C, et al. Neurologic outcomes after extracorporeal membrane oxygenation: a systematic review. Pediatr Crit Care Med 2018;19:760-6. https://doi.org/10.1097/PCC.0000000000001612
  70. Xiong H, Xia B, Zhu J, Li B, Huang W. Clinical outcomes in pediatric patients hospitalized with fulminant myocarditis requiring extracorporeal membrane oxygenation: a meta-analysis. Pediatr Cardiol 2017;38:209-14. https://doi.org/10.1007/s00246-016-1517-1
  71. Wilmot I, Morales DL, Price JF, Rossano JW, Kim JJ, Decker JA, et al. Effectiveness of mechanical circulatory support in children with acute fulminant and persistent myocarditis. J Card Fail 2011;17:487-94. https://doi.org/10.1016/j.cardfail.2011.02.008
  72. Sadhwani A, Cheng H, Stopp C, Rollins CK, Jolley MA, Dunbar-Masterson C, et al. Early neurodevelopmental outcomes in children supported with ECMO for cardiac indications. Pediatr Cardiol 2019;40:1072-83. https://doi.org/10.1007/s00246-019-02115-1
  73. Schlapbach LJ, Chiletti R, Straney L, Festa M, Alexander D, Butt W, et al. Defining benefit threshold for extracorporeal membrane oxygenation in children with sepsis-a binational multicenter cohort study. Critical Care (London, England) 2019;23:429. https://doi.org/10.1186/s13054-019-2685-1
  74. Kociol RD, Cooper LT, Fang JC, Moslehi JJ, Pang PS, Sabe MA, et al. Recognition and initial management of fulminant myocarditis: a scientific statement from the American Heart Association. Circulation 2020;141:e69-92.
  75. Lee EY, Lee HL, Kim HT, Lee HD, Park JA. Clinical features and short-term outcomes of pediatric acute fulminant myocarditis in a single center. Korean J Pediatr 2014;57:489-95. https://doi.org/10.3345/kjp.2014.57.11.489
  76. Nosaka N, Muguruma T, Fujiwara T, Enomoto Y, Toida C, Morishima T. Effects of the elective introduction of extracorporeal membrane oxygenation on outcomes in pediatric myocarditis cases. Acute Med Surg 2014;2:92-7. https://doi.org/10.1002/ams2.76
  77. Sik G, Annayev A, Demirbuga A, Deliceo E, Aydin S, Erek E, et al. Extracorporeal membrane oxygenation for the support of pediatric patients with acute fulminant myocarditis. Turk J Pediatr 2019;61:867-72. https://doi.org/10.24953/turkjped.2019.06.007

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