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Lymphatic anomalies in congenital heart disease

  • Thoracic imaging
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Abstract

Congenital heart disease can lead to various lymphatic complications including traumatic leaks, lymphatic overproduction, conduction abnormalities or lymphedema. Advancements in the imaging of central lymphatics and guided interventions have improved outcomes in these children. Dynamic contrast-enhanced magnetic resonance (MR) lymphangiography allows for the assessment of abnormal lymphatic drainage. This technique is preferred for evaluating lymphatic conditions such as plastic bronchitis, chylothorax, chyloptysis, chylopericardium, protein-losing enteropathy and chylous ascites, among other lymphatic disorders. In this review, we discuss lymphatic abnormalities encountered on MRI in children with congenital heart disease. We also briefly review treatment options.

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References

  1. Kelly B, Mohanakumar S, Hjortdal VE (2020) Diagnosis and management of lymphatic disorders in congenital heart disease. Curr Cardiol Rep 22:164

    Article  PubMed  PubMed Central  Google Scholar 

  2. Rapp JB, White AM, Otero HJ, Biko DM (2021) Computed tomography of the airways and lungs in congenital heart disease. Pediatr Radiol. https://doi.org/10.1007/s00247-021-05186-6

    Article  PubMed  Google Scholar 

  3. Itkin M, Chidekel A, Ryan KA, Rabinowitz D (2020) Abnormal pulmonary lymphatic flow in patients with paediatric pulmonary lymphatic disorders: diagnosis and treatment. Paediatr Respir Rev 36:15–24

    PubMed  Google Scholar 

  4. Dori Y, Keller MS, Rychik J, Itkin M (2014) Successful treatment of plastic bronchitis by selective lymphatic embolization in a Fontan patient. Pediatrics 134:e590–595

    Article  PubMed  Google Scholar 

  5. Ramirez-Suarez KI, Tierradentro-Garcia LO, Smith CL et al (2021) Dynamic contrast-enhanced magnetic resonance lymphangiography. Pediatr Radiol 52:285–294

    Article  PubMed  Google Scholar 

  6. Butler MG, Isogai S, Weinstein BM (2009) Lymphatic development. Birth Defects Res C Embryo Today 87:222–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Tomasulo CE, Chen JM, Smith CL et al (2020) Lymphatic disorders and management in patients with congenital heart disease. Ann Thorac Surg 113:1101–1111

    Article  PubMed  Google Scholar 

  8. Shaikh R, Biko DM, Lee EY (2019) MR imaging evaluation of pediatric lymphatics: overview of techniques and imaging findings. Magn Reson Imaging Clin N Am 27:373–385

    Article  PubMed  Google Scholar 

  9. Johnson OW, Chick JFB, Chauhan NR et al (2016) The thoracic duct: clinical importance, anatomic variation, imaging, and embolization. Eur Radiol 26:2482–2493

    Article  PubMed  Google Scholar 

  10. Biko DM, Johnstone JA, Dori Y et al (2018) Recognition of neonatal lymphatic flow disorder: fetal MR findings and postnatal MR lymphangiogram correlation. Acad Radiol 25:1446–1450

    Article  PubMed  Google Scholar 

  11. Biko DM, Reisen B, Otero HJ et al (2019) Imaging of central lymphatic abnormalities in Noonan syndrome. Pediatr Radiol 49:586–592

    Article  PubMed  Google Scholar 

  12. Lam CZ, Bhamare TA, Gazzaz T et al (2017) Diagnosis of secondary pulmonary lymphangiectasia in congenital heart disease: a novel role for chest ultrasound and prognostic implications. Pediatr Radiol 47:1441–1451

    Article  PubMed  Google Scholar 

  13. Bellini C, Boccardo F, Campisi C, Bonioli E (2006) Congenital pulmonary lymphangiectasia. Orphanet J Rare Dis 1:43

    Article  PubMed  PubMed Central  Google Scholar 

  14. Seed M, Bradley T, Bourgeois J et al (2009) Antenatal MR imaging of pulmonary lymphangiectasia secondary to hypoplastic left heart syndrome. Pediatr Radiol 39:747–749

    Article  PubMed  Google Scholar 

  15. Barrera CA, Johnson AM, Rychik J et al (2021) Prognostic value of the nutmeg lung pattern/lymphangiectasia on fetal magnetic resonance imaging. Pediatr Radiol 51:1809–1817

    Article  PubMed  Google Scholar 

  16. Victoria T, Andronikou S (2014) The fetal MR appearance of “nutmeg lung”: findings in 8 cases linked to pulmonary lymphangiectasia. Pediatr Radiol 44:1237–1242

    Article  PubMed  Google Scholar 

  17. Itkin M, Rabinowitz DA, Nadolski G et al (2020) Abnormal pulmonary lymphatic flow in patients with lymphatic anomalies and respiratory compromise. Chest 158:681–691

    Article  PubMed  Google Scholar 

  18. Barrera CA, Victoria T, Escobar FA et al (2020) Imaging of fetal lymphangiectasias: prenatal and postnatal imaging findings. Pediatr Radiol 50:1872–1880

    Article  PubMed  Google Scholar 

  19. Chavhan GB, Amaral JG, Temple M, Itkin M (2017) MR lymphangiography in children: technique and potential applications. Radiographics 37:1775–1790

    Article  PubMed  Google Scholar 

  20. Pinto E, Dori Y, Smith C et al (2021) Neonatal lymphatic flow disorders: impact of lymphatic imaging and interventions on outcomes. J Perinatol 41:494–501

    Article  CAS  PubMed  Google Scholar 

  21. Savla JJ, Itkin M, Rossano JW, Dori Y (2017) Post-operative chylothorax in patients with congenital heart disease. J Am Coll Cardiol 69:2410–2422

    Article  PubMed  Google Scholar 

  22. Ahmed MA (2021) Post-operative chylothorax in children undergoing congenital heart surgery. Cureus 13:e13811

    PubMed  PubMed Central  Google Scholar 

  23. Mery CM, Moffett BS, Khan MS et al (2014) Incidence and treatment of chylothorax after cardiac surgery in children: analysis of a large multi-institution database. J Thorac Cardiovasc Surg 147:678–686e1

    Article  PubMed  Google Scholar 

  24. Fredenburg TB, Johnson TR, Cohen MD (2011) The Fontan procedure: anatomy, complications, and manifestations of failure. Radiographics 31:453–463

    Article  PubMed  Google Scholar 

  25. Khanna G, Bhalla S, Krishnamurthy R, Canter C (2012) Extracardiac complications of the Fontan circuit. Pediatr Radiol 42:233–241

    Article  PubMed  Google Scholar 

  26. Ghosh RM, Griffis HM, Glatz AC et al (2020) Prevalence and cause of early Fontan complications: does the lymphatic circulation play a role? J Am Heart Assoc 9:e015318

    Article  PubMed  PubMed Central  Google Scholar 

  27. Dori Y, Keller MS, Fogel MA et al (2014) MRI of lymphatic abnormalities after functional single-ventricle palliation surgery. AJR Am J Roentgenol 203:426–431

    Article  PubMed  Google Scholar 

  28. Menon S, Chennapragada M, Ugaki S et al (2017) The lymphatic circulation in adaptations to the Fontan circulation. Pediatr Cardiol 38:886–892

    Article  PubMed  Google Scholar 

  29. Witte MH, Dumont AE, Clauss RH et al (1969) Lymph circulation in congestive heart failure: effect of external thoracic duct drainage. Circulation 39:723–733

    Article  CAS  PubMed  Google Scholar 

  30. Milonakis M, Chatzis AC, Giannopoulos NM et al (2009) Etiology and management of chylothorax following pediatric heart surgery. J Card Surg 24:369–373

    Article  PubMed  Google Scholar 

  31. Schumacher KR, Stringer KA, Donohue JE et al (2015) Fontan-associated protein-losing enteropathy and plastic bronchitis. J Pediatr 166:970–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Talwar S, Agarwala S, Mittal CM et al (2010) Pleural effusions in children undergoing cardiac surgery. Ann Pediatr Cardiol 3:58–64

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kim G, Ko H, Byun J-H et al (2019) Risk factors for prolonged pleural effusion after extracardiac Fontan operation. Pediatr Cardiol 40:1545–1552

    Article  PubMed  Google Scholar 

  34. Itkin M, Piccoli DA, Nadolski G et al (2017) Protein-losing enteropathy in patients with congenital heart disease. J Am Coll Cardiol 69:2929–2937

    Article  CAS  PubMed  Google Scholar 

  35. Lemley BA, Biko DM, Dewitt AG et al (2021) Intrahepatic dynamic contrast-enhanced magnetic resonance lymphangiography: potential imaging signature for protein-losing enteropathy in congenital heart disease. J Am Heart Assoc 10:e021542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sagray E, Johnson JN, Schumacher KR et al (2022) Protein-losing enteropathy recurrence after pediatric heart transplantation: multicenter case series. Pediatr Transplant 2022:e14295

  37. Biko DM, Dori Y, Savoca M et al (2020) Pediatric pulmonary lymphatic flow disorders: diagnosis and management. Paediatr Respir Rev 36:2–7

    PubMed  Google Scholar 

  38. Ramirez-Suarez KI, Otero HJ, Biko DM et al (2022) Magnetic resonance lymphangiography in post-Fontan palliation patients with MR non-conditional cardiac electronic devices: an institutional experience. Clin Imaging 86:43–52

    Article  PubMed  Google Scholar 

  39. Dori Y, Smith CL, DeWitt AG et al (2020) Intramesenteric dynamic contrast pediatric MR lymphangiography: initial experience and comparison with intranodal and intrahepatic MR lymphangiography. Eur Radiol 30:5777–5784

    Article  CAS  PubMed  Google Scholar 

  40. Biko DM, Smith CL, Otero HJ et al (2019) Intrahepatic dynamic contrast MR lymphangiography: initial experience with a new technique for the assessment of liver lymphatics. Eur Radiol 29:5190–5196

    Article  PubMed  Google Scholar 

  41. Nadolski GJ, Ponce-Dorrego MD, Darge K et al (2018) Validation of the position of injection needles with contrast-enhanced ultrasound for dynamic contract-enhanced MR lymphangiography. J Vasc Interv Radiol 29:1028–1030

    Article  PubMed  Google Scholar 

  42. Dori Y (2016) Novel lymphatic imaging techniques. Tech Vasc Interv Radiol 19:255–261

    Article  PubMed  Google Scholar 

  43. Dori Y, Keller MS, Rome JJ et al (2016) Percutaneous lymphatic embolization of abnormal pulmonary lymphatic flow as treatment of plastic bronchitis in patients with congenital heart disease. Circulation 133:1160–1170

    Article  PubMed  Google Scholar 

  44. Mon RA, Treadwell MC, Berman DR et al (2018) Outcomes of fetuses with primary hydrothorax that undergo prenatal intervention (prenatal intervention for hydrothorax). J Surg Res 221:121–127

    Article  PubMed  Google Scholar 

  45. Carr BD, Sampang L, Church JT et al (2018) Fetal intervention for congenital chylothorax is associated with improved outcomes in early life. J Surg Res 231:361–365

    Article  PubMed  Google Scholar 

  46. Desai AP, Guvenc BH, Carachi R (2009) Evidence for medium chain triglycerides in the treatment of primary intestinal lymphangiectasia. Eur J Pediatr Surg 19:241–245

    Article  CAS  PubMed  Google Scholar 

  47. Panthongviriyakul C, Bines JE (2008) Post-operative chylothorax in children: an evidence-based management algorithm. J Paediatr Child Health 44:716–721

    Article  PubMed  Google Scholar 

  48. Brooks K, Caruthers RL, Schumacher KR, Stringer KA (2013) Pharmacotherapy challenges of Fontan-associated plastic bronchitis: a rare pediatric disease. Pharmacotherapy 33:922–934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Heath L, Ling S, Racz J et al (2011) Prospective, longitudinal study of plastic bronchitis cast pathology and responsiveness to tissue plasminogen activator. Pediatr Cardiol 32:1182–1189

    Article  PubMed  PubMed Central  Google Scholar 

  50. Avitabile CM, Goldberg DJ, Dodds K et al (2014) A multifaceted approach to the management of plastic bronchitis after cavopulmonary palliation. Ann Thorac Surg 98:634–640

    Article  PubMed  PubMed Central  Google Scholar 

  51. Li D, March ME, Gutierrez-Uzquiza A et al (2019) ARAF recurrent mutation causes central conducting lymphatic anomaly treatable with a MEK inhibitor. Nat Med 25:1116–1122

    Article  CAS  PubMed  Google Scholar 

  52. Ozeki M, Hori T, Kanda K et al (2016) Everolimus for primary intestinal lymphangiectasia with protein-losing enteropathy. Pediatrics 137:e20152562

    Article  PubMed  Google Scholar 

  53. Kuroiwa G, Takayama T, Sato Y et al (2001) Primary intestinal lymphangiectasia successfully treated with octreotide. J Gastroenterol 36:129–132

    Article  CAS  PubMed  Google Scholar 

  54. Gray M, Kovatis KZ, Stuart T et al (2014) Treatment of congenital pulmonary lymphangiectasia using ethiodized oil lymphangiography. J Perinatol 34:720–722

    Article  CAS  PubMed  Google Scholar 

  55. Hraška V (2013) Decompression of thoracic duct: new approach for the treatment of failing Fontan. Ann Thorac Surg 96:709–711

    Article  PubMed  Google Scholar 

  56. Smith CL, Hoffman TM, Dori Y, Rome JJ (2020) Decompression of the thoracic duct: a novel transcatheter approach. Catheter Cardiovasc Interv 95:E56–E61

    PubMed  Google Scholar 

  57. Attar MA, Donn SM (2017) Congenital chylothorax. Semin Fetal Neonatal Med 22:234–239

    Article  PubMed  Google Scholar 

  58. Engum SA, Rescorla FJ, West KW et al (1999) The use of pleuroperitoneal shunts in the management of persistent chylothorax in infants. J Pediatr Surg 34:286–290

    Article  CAS  PubMed  Google Scholar 

  59. Kogon B, McConnell M, Book W (2016) Fontan conversion with hepatic vein exclusion: a means for hepatic preservation in single ventricle heart disease. Cardiol Young 26:582–585

    Article  PubMed  Google Scholar 

  60. Hayashida K, Yamakawa S, Shirakami E (2019) Lymphovenous anastomosis for the treatment of persistent congenital chylothorax in a low-birth-weight infant. Medicine 98:e17575

    Article  PubMed  PubMed Central  Google Scholar 

  61. Weissler JM, Cho EH, Koltz PF et al (2018) Lymphovenous anastomosis for the treatment of chylothorax in infants: a novel microsurgical approach to a devastating problem. Plast Reconstr Surg 141:1502–1507

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Radiology, Children’s Hospital of Philadelphia, 3401 Civic Center Blvd., Philadelphia, PA, 19104, USA

    Karen I. Ramirez-Suarez, Luis Octavio Tierradentro-García, David M. Biko, Hansel J. Otero, Ammie M. White, Seth Vatsky & Jordan B. Rapp

  2. Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    David M. Biko, Hansel J. Otero, Ammie M. White, Yoav Dori, Christopher L. Smith, Seth Vatsky & Jordan B. Rapp

  3. Division of Cardiology, Department of Pediatrics, Children’s Hospital of Philadelphia, Philadelphia, PA, USA

    Yoav Dori & Christopher L. Smith

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  1. Karen I. Ramirez-Suarez
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  2. Luis Octavio Tierradentro-García
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Correspondence to Jordan B. Rapp.

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Ramirez-Suarez, K.I., Tierradentro-García, L.O., Biko, D.M. et al. Lymphatic anomalies in congenital heart disease. Pediatr Radiol 52, 1862–1876 (2022). https://doi.org/10.1007/s00247-022-05449-w

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