Abstract
Endomyocardial biopsy (EMB) is a common procedure used to aid in the diagnosis, prognosis and treatment of suspected pediatric cardiomyopathy. In suspected cardiomyopathy, no multicenter experience has previously reported on the safety and utility of EMBs. Retrospectively, adverse event (AE) and patient and procedural characteristics were obtained at seven institutions participating in the Congenital Cardiac Catheterization Outcomes Project for both a cardiomyopathy (n = 158) and a post-transplant surveillance (n = 2665) cohort. Descriptive information regarding biopsy indication, pathology and clinical management based on EMB findings were retrospectively obtained. High-severity AEs were more common in the cardiomyopathy cohort when compared to the post-transplant surveillance cohort. The cardiomyopathy cohort was younger, more hemodynamically vulnerable and required more cardiorespiratory support during the procedure. The eight high-severity AEs in the cardiomyopathy group included one myocardial perforation, two ECMO cannulations and three deaths following the EMB. Factors associated with high-severity AEs included performing another catheter-based intervention during the EMB and longer fluoroscopy time. Notably, an increased number of biopsy attempts did not increase the risk of an AE. Suspected myocarditis was the most common indication. Diagnostic EMB pathology and thus alteration to clinical management based on pathology occurred more frequently in patients with suspected myocarditis. In conclusion, there is an increased incidence of high-severity AEs in patients undergoing EMB for suspected cardiomyopathy. EMB may be more clinically useful in the management of suspected myocarditis. The increased risk of high-severity AEs when additional interventions are performed highlights the hemodynamic vulnerability in patients with suspected cardiomyopathy.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Maron BJ, Towbin JA, Thiene G, Antzelevitch C, Corrado D, Arnett D et al (2006) Contemporary definitions and classification of the cardiomyopathies: an American Heart Association Scientific Statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention. Circulation 113(14):1807–1816
Felker GM, Thompson RE, Hare JM, Hruban RH, Clemetson DE, Howard DL et al (2000) Underlying causes and long-term survival in patients with initially unexplained cardiomyopathy. N Engl J Med 342(15):1077–1084
Wilkinson JD, Landy DC, Colan SD, Towbin JA, Sleeper LA, Orav EJ et al (2010) The pediatric cardiomyopathy registry and heart failure: key results from the first 15 years. Heart Fail Clin 6(4):401–413
Cooper LT, Baughman KL, Feldman AM, Frustaci A, Jessup M, Kuhl U et al (2007) The role of endomyocardial biopsy in the management of cardiovascular disease: a scientific statement from the American Heart Association, the American College of Cardiology, and the European Society of Cardiology. Endorsed by the Heart Failure Society of America and the Heart Failure Association of the European Society of Cardiology. J Am Coll Cardiol 50(19):1914–1931
Zhorne D, Petit CJ, Ing FF, Justino H, Jefferies JL, Dreyer WJ et al (2013) A 25-year experience of endomyocardial biopsy safety in infants. Catheter Cardiovasc Interv 82(5):797–801
Schmaltz AA, Apitz J, Hort W, Maisch B (1990) Endomyocardial biopsy in infants and children: experience in 60 patients. Pediatr Cardiol 11(1):15–21
Pophal SG, Sigfusson G, Booth KL, Bacanu SA, Webber SA, Ettedgui JA et al (1999) Complications of endomyocardial biopsy in children. J Am Coll Cardiol 34(7):2105–2110
Yoshizato T, Edwards WD, Alboliras ET, Hagler DJ, Driscoll DJ (1990) Safety and utility of endomyocardial biopsy in infants, children and adolescents: a review of 66 procedures in 53 patients. J Am Coll Cardiol 15(2):436–442
Bergersen L, Gauvreau K, Jenkins KJ, Lock JE (2008) Adverse event rates in congenital cardiac catheterization: a new understanding of risks. Congenit Heart Dis 3(2):90–105
Bergersen L, Marshall A, Gauvreau K, Beekman R, Hirsch R, Foerster S et al (2010) Adverse event rates in congenital cardiac catheterization—a multi-center experience. Catheter Cardiovasc Interv 75(3):389–400
Daly KP, Marshall AC, Vincent JA, Zuckerman WA, Hoffman TM, Canter CE et al (2012) Endomyocardial biopsy and selective coronary angiography are low-risk procedures in pediatric heart transplant recipients: results of a multicenter experience. J Heart Lung Transplant 31(4):398–409
Leatherbury L, Chandra RS, Shapiro SR, Perry LW (1988) Value of endomyocardial biopsy in infants, children and adolescents with dilated or hypertrophic cardiomyopathy and myocarditis. J Am Coll Cardiol 12(6):1547–1554
Chin C, Akhtar MJ, Rosenthal DN, Bernstein D (2000) Safety and utility of the routine surveillance biopsy in pediatric patients 2 years after heart transplantation. J Pediatr 136(2):238–242
Cowley CG, Lozier JS, Orsmond GS, Shaddy RE (2003) Safety of endomyocardial biopsy in children. Cardiol Young 13(5):404–407
Lurie PR, Fujita M, Neustein HB (1978) Transvascular endomyocardial biopsy in infants and small children: description of a new technique. Am J Cardiol 42(3):453–457
Shaddy RE, Bullock EA (1993) Efficacy of 100 consecutive right ventricular endomyocardial biopsies in pediatric patients using the right internal jugular venous approach. Pediatr Cardiol 14(1):5–8
Eastaugh LJ, Thiagarajan RR, Darst JR, McElhinney DB, Lock JE, Marshall AC (2015) Percutaneous left atrial decompression in patients supported with extracorporeal membrane oxygenation for cardiac disease. Pediatr Crit Care Med 16:59–65
Holzmann M, Nicko A, Kuhl U, Noutsias M, Poller W, Hoffmann W et al (2008) Complication rate of right ventricular endomyocardial biopsy via the femoral approach: a retrospective and prospective study analyzing 3048 diagnostic procedures over an 11-year period. Circulation 118(17):1722–1728
Chen RJ, Wei J, Chang CY, Chuang YC, Lee KC, Sue SH et al (2008) Tricuspid valve regurgitation and endomyocardial biopsy after orthotopic heart transplantation. Transplant Proc 40(8):2603–2606
McCreery CJ, McCulloch M, Ahmad M, deFilippi CR (2001) Real-time 3-dimensional echocardiography imaging for right ventricular endomyocardial biopsy: a comparison with fluoroscopy. J Am Soc Echocardiogr 14(9):927–933
Ghelani SJ, Spaeder MC, Pastor W, Spurney CF, Klugman D (2012) Demographics, trends, and outcomes in pediatric acute myocarditis in the United States, 2006 to 2011. Circ Cardiovasc Qual Outcomes 5(5):622–627
Gagliardi MG, Bevilacqua M, Di Renzi P, Picardo S, Passariello R, Marcelletti C (1991) Usefulness of magnetic resonance imaging for diagnosis of acute myocarditis in infants and children, and comparison with endomyocardial biopsy. Am J Cardiol 68(10):1089–1091
Friedrich MG, Strohm O, SchulzMenger J, Marciniak H, Luft FC, Dietz R (1998) Contrast media-enhanced magnetic resonance imaging visualizes myocardial changes in the course of viral myocarditis. Circulation 97:1802–1809
Laissy JP, Messin B, Varenne O et al (2002) MRI of acute myocarditis: a comprehensive approach based on various imaging sequences. Chest 122:1638–1648
Mahrholdt H, Goedecke C, Wagner A et al (2004) Cardiovascular magnetic resonance assessment of human myocarditis: a comparison to histology and molecular pathology. Circulation 109:1250–1258
Abdel-Aty H, Boye P, Zagrosek A et al (2005) Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol 45:1815–1822
Gutberlet M, Spors B, Thoma T et al (2008) Suspected chronic myocarditis at cardiac MR: diagnostic accuracy and association with immunohistologically detected inflammation and viral persistence. Radiology 246:401–409
Roditi GH, Hartnell GC, Cohen MC (2000) MRI changes in myocarditis—evaluation with spin echo, cine MR angiography and contrast enhanced spin echo imaging. Clin Radiol 55:752–758
Rieker O, Mohrs O, Oberholzer K, Kreitner KF, Thelen M (2002) Cardiac MRI in suspected myocarditis. Rofo Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr. 174:1530–1536
Laissy JP, Hyafil F, Feldman LJ et al (2005) Differentiating acute myocardial infarction from myocarditis: diagnostic value of early- and delayed-perfusion cardiac MR imaging. Radiology 237:75–82
Ingkanisorn WP, Paterson DI, Calvo KR et al (2006) Cardiac magnetic resonance appearance of myocarditis caused by high dose IL-2: similarities to community-acquired myocarditis. J Cardiovasc Magn Reson 8:353–360
De Cobelli F, Pieroni M, Esposito A et al (2006) Delayed gadolinium-enhanced cardiac magnetic resonance in patients with chronic myocarditis presenting with heart failure or recurrent arrhythmias. J Am Coll Cardiol 47:1649–1654
Mahrholdt H, Wagner A, Deluigi CC et al (2006) Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation 114:1581–1590
Schulz-Menger J, Wassmuth R, Abdel-Aty H et al (2006) Patterns of myocardial inflammation and scarring in sarcoidosis as assessed by cardiovascular magnetic resonance. Heart 92:399–400
Yelgec NS, Dymarkowski S, Ganame J, Bogaert J (2007) Value of MRI in patients with a clinical suspicion of acute myocarditis. Eur Radiol 17:2211–2217
Yilmaz A, Mahrholdt H, Athanasiadis A et al (2008) Coronary vasospasms the underlying cause for chest pain in patients with PVB19-myocarditis. Heart 94:1456–1463
Wagner A, Schulz-Menger J, Dietz R, Friedrich MG (2003) Longterm follow-up of patients with acute myocarditis by magnetic resonance imaging. Magma 16:17–20
Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, White JA, Abdel-Aty H, Gutberlet M, Prasad S, Aletras A, Laissy JP, Paterson I, Filipchuk NG, Kumar A, Pauschinger M, Liu P (2009) Cardiovascular magnetic resonance in myocarditis: a JACC white paper. J Am Coll Cardiol 53:1475–1487
Feldman AM, McNamara D (2000) Medical progress: myocarditis. N Engl J Med 343:1388–1398
Baughman KL (2006) Diagnosis of myocarditis: death of Dallas criteria. Circulation 113:593–595
Shanes JG, Ghali J, Billingham ME et al (1987) Interobserver variability in the pathologic interpretation of endomyocardial biopsy results. Circulation 75:401–405
Daubeney PE, Nugent AW, Chondros P, Carlin JB, Colan SD, Cheung M et al (2006) Clinical features and outcomes of childhood dilated cardiomyopathy: results from a national population-based study. Circulation 114(24):2671–2678
Hill KD, Atkinson JB, Doyle TP, Dodd D (2009) Routine performance of endomyocardial biopsy decreases the incidence of orthotopic heart transplant for myocarditis. J Heart Lung Transplant 28(12):1261–1266
Acknowledgments
Dr. Daly has been supported by NIH Grants L40 HL110356, T32 HL07572, and K12 HD052896-06, the Alexia Clinton Research Fund, and the Boston Children’s Hospital Cardiac Transplant and Education Fund.
Author’s Contributions
Kimberly I. Mills contributed to data analysis, drafting article and statistics; Julie A. Vincent, Warren A. Zuckerman, Timothy M. Hoffman, Charles E. Canter, Audrey C. Marshall, Elizabeth D. Blume helped in data collection, study design, revision of article; Lisa Bergersen contributed to overall database design, study design and critical revision of article; and Kevin P. Daly helped in study concept and design, data collection and critical revision of article.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no financial or professional disclosures to report related to any of the data presented herein.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Appendix: Study Sites and Participants
Appendix: Study Sites and Participants
Children’s Hospital Boston: Lisa Bergersen, MD, MPH, Michael Landzberg, MD, Peter Lang, MD, James Lock, MD, Audrey Marshall, MD, and Doff McElhinney, MD.
Cincinnati Children’s Hospital Medical Center: Robert Beekman, MD, and Russel Hirsch, MD.
Morgan Stanley Children’s Hospital of New York Presbyterian: William Hellenbrand, MD, Julie Vincent, MD, and Alejandro Torres, MD.
Nationwide Children’s Hospital: John Cheatham, MD, Ralf Holzer, MD, and Timothy Hoffman, MD.
St. Louis Children’s Hospital: David Balzer, MD, Susan Foerster, MD, Ramzi Nicolas, MD, and Joshua Murphy, MD.
Rady Children’s Hospital—San Diego: John Moore, MD, and Howaida El-Said, MD.
Pittsburgh Children’s Hospital: Jacqueline Kreutzer, MD, Sara Trucco, MD, Brian Feingold, MD, Susan Miller, MD, and Lee Berman, MD.
Oregon Health Sciences University: Grant Burch, MD, and Laurie Armsby, MD.
Rights and permissions
About this article
Cite this article
Mills, K.I., Vincent, J.A., Zuckerman, W.A. et al. Is Endomyocardial Biopsy a Safe and Useful Procedure in Children with Suspected Cardiomyopathy?. Pediatr Cardiol 37, 1200–1210 (2016). https://doi.org/10.1007/s00246-016-1416-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00246-016-1416-5