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Pediatric Radiology

, Volume 35, Issue 3, pp 258–274 | Cite as

Pulmonary thromboembolism in children

  • Paul S. Babyn
  • Harpal K. Gahunia
  • Patricia Massicotte
Review

Abstract

Pulmonary thromboembolism (PTE) is uncommonly diagnosed in the pediatric patient, and indeed often only discovered on autopsy. The incidence of pediatric PTE depends upon the associated underlying disease, diagnostic tests used, and index of suspicion. Multiple risk factors can be found including: peripartum asphyxia, dyspnea, haemoptysis, chest pain, dehydration, septicemia, central venous lines (CVLs), trauma, surgery, ongoing hemolysis, vascular lesions, malignancy, renal disease, foreign bodies or, uncommonly, intracranial venous sinus thrombosis, burns, or nonbacterial thrombotic endocarditis. Other types of embolism can occur uncommonly in childhood and need to be recognized, as the required treatment will vary. These include pulmonary cytolytic thrombi, foreign bodies, tumor and septic emboli, and post-traumatic fat emboli. No single noninvasive test for pulmonary embolism is both sensitive and specific. A combination of diagnostic procedures must be used to identify suspect or confirmed cases of PTE. This article reviews the risk factors, clinical presentation and treatment of pulmonary embolism in children. It also highlights the current diagnostic tools and protocols used to evaluate pulmonary embolism in pediatric patients.

Keywords

Children Pulmonary Embolus Thrombus CT 

Notes

Acknowledgements

We wish to thank Dr. Mustafa Khan and Dr. Judith Ash for their valuable suggestions.

References

  1. 1.
    Becker RC, Graor R, Holloway J (1984) Pulmonary embolism: a review of 200 cases with emphasis on pathophysiology, diagnosis, and treatment. Cleve Clin Q 51:519–529PubMedGoogle Scholar
  2. 2.
    Rubinstein I, Murray D, Hoffstein V (1988) Fatal pulmonary emboli in hospitalized patients. An autopsy study. Arch Intern Med 148:1425–1426CrossRefPubMedGoogle Scholar
  3. 3.
    Monagle P, Adams M, Mahoney M, et al (2000) Outcome of pediatric thromboembolic disease: a report from the Canadian Childhood Thrombophilia Registry. Pediatr Res 47:763–766PubMedGoogle Scholar
  4. 4.
    Andrew M, David M, Adams M, et al (1994) Venous thromboembolic complications (VTE) in children: first analyses of the Canadian Registry of VTE. Blood 83:1251–1257PubMedGoogle Scholar
  5. 5.
    Morrell MT, Dunnill MS (1968) The post-mortem incidence of pulmonary embolism in a hospital population. Br J Surg 55:347–352PubMedGoogle Scholar
  6. 6.
    Dollery CM, Sullivan ID, Bauraind O, et al (1994) Thrombosis and embolism in long-term central venous access for parenteral nutrition. Lancet 344:1043–1045CrossRefPubMedGoogle Scholar
  7. 7.
    Hoyer PF, Gonda S, Barthels M, et al (1986) Thromboembolic complications in children with nephrotic syndrome. Risk and incidence. Acta Paediatr Scand 75:804–810PubMedGoogle Scholar
  8. 8.
    Schlegel N (1997) Thromboembolic risks and complications in nephrotic children. Semin Thromb Hemost 23:271–280PubMedGoogle Scholar
  9. 9.
    Byard RW, Cutz E (1990) Sudden and unexpected death in infancy and childhood due to pulmonary thromboembolism. An autopsy study. Arch Pathol Lab Med 114:142–144PubMedGoogle Scholar
  10. 10.
    Buck JR, Connors RH, Coon WW, et al (1981) Pulmonary embolism in children. J Pediatr Surg 16:385–391PubMedGoogle Scholar
  11. 11.
    Chan AK, Deveber G, Monagle P, et al (2003) Venous thrombosis in children. J Thromb Haemost 1:1443–1455CrossRefPubMedGoogle Scholar
  12. 12.
    Anton N, Massicotte MP (2001) Venous thromboembolism in pediatrics. Semin Vasc Surg 1:111–122Google Scholar
  13. 13.
    Zimmerman RL, Novek S, Chen JT, et al (1994) Pulmonary thrombosis in a 10-year-old child with minimal change disease and nephrotic syndrome. A clinical, radiologic, and pathologic correlation with literature review. Am J Clin Pathol 101:230–236PubMedGoogle Scholar
  14. 14.
    Sonakul D, Fucharoen S (1992) Pulmonary thromboembolism in thalassemic patients. Southeast Asian J Trop Med Public Health 23:25–28PubMedGoogle Scholar
  15. 15.
    Rogers JS 2nd (1993) Hypercoagulable states. W V Med J 89:61–63PubMedGoogle Scholar
  16. 16.
    Nielsen HK (1991) Pathophysiology of venous thromboembolism. Semin Thromb Hemost 17(Suppl 3):250–253PubMedGoogle Scholar
  17. 17.
    Schmidt B, Andrew M (1995) Neonatal thrombosis: report of a prospective Canadian and international registry. Pediatrics 96:939–943PubMedGoogle Scholar
  18. 18.
    Heller C, Schobess R, Kurnik K, et al (2000) Abdominal venous thrombosis in neonates and infants: role of prothrombotic risk factors – a multicentre case-control study. For the Childhood Thrombophilia Study Group. Br J Haematol 111:534–539CrossRefPubMedGoogle Scholar
  19. 19.
    Streif W, Andrew ME (1998) Venous thromboembolic events in pediatric patients. Diagnosis and management. Hematol Oncol Clin North Am 12:1283–1312 viiPubMedGoogle Scholar
  20. 20.
    van Ommen CH, Heijboer H, Buller HR, et al (2001) Venous thromboembolism in childhood: a prospective two-year registry in The Netherlands. J Pediatr 139:676–681CrossRefPubMedGoogle Scholar
  21. 21.
    Massicotte MP, Dix D, Monagle P, et al (1998) Central venous catheter-related thrombosis in children: analysis of the Canadian Registry of Venous Thromboembolic Complications. J Pediatr 133:770–776PubMedGoogle Scholar
  22. 22.
    Yuen SY, Lau KF, Steinberg AW, et al (2001) Intracranial venous thrombosis and pulmonary embolism with antiphospholipid syndrome in systemic lupus erythematosus. J Paediatr Child Health 37:405–408Google Scholar
  23. 23.
    Case records of the Massachusetts General Hospital (1980) Weekly clinicopathological exercises. Case 27-1980. N Engl J Med 303:92–100PubMedGoogle Scholar
  24. 24.
    Prandoni P, Lensing AW, Cogo A, et al (1996) The long-term clinical course of acute deep venous thrombosis. Ann Intern Med 125:1–7PubMedGoogle Scholar
  25. 25.
    Male C, Chait P, Andrew M, et al (2003) Central venous line-related thrombosis in children: association with central venous line location and insertion technique. Blood 101:4273–4278CrossRefPubMedGoogle Scholar
  26. 26.
    Andrew M, Investigators P (2000) A randomized control trial of low molecular weight heparin for the prevention of central venous line-related thrombotic complications in children: The PROTEKT Trial. Blood 96(Suppl):492aGoogle Scholar
  27. 27.
    Emery JL, Hilton HB (1961) Lung and heart complications of the treatment of hydrocephalus by ventriculoauriculostomy. Surgery 50:309–314PubMedGoogle Scholar
  28. 28.
    Haber SL, Bennington JL (1962) Pulmonary embolism in an infant. J Pediatr 61:759–762PubMedGoogle Scholar
  29. 29.
    David M, Andrew M (1993) Venous thromboembolic complications in children. J Pediatr 123:337–346PubMedGoogle Scholar
  30. 30.
    Jones DR, Macintyre IM (1975) Venous thromboembolism in infancy and childhood. Arch Dis Child 50:153–155Google Scholar
  31. 31.
    Burihan E, de Figueiredo LF, Francisco J Jr, et al (1993) Upper-extremity deep venous thrombosis: analysis of 52 cases. Cardiovasc Surg 1:19–22PubMedGoogle Scholar
  32. 32.
    Andrew M, Marzinotto V, Pencharz P, et al (1995) A cross-sectional study of catheter-related thrombosis in children receiving total parenteral nutrition at home. J Pediatr 126:358–363PubMedGoogle Scholar
  33. 33.
    Hassall E, Ulich T, Ament ME (1983) Pulmonary embolus and Malassezia pulmonary infection related to urokinase therapy. J Pediatr 102:722–725PubMedGoogle Scholar
  34. 34.
    Rockoff MA, Gang DL, Vacanti JP (1984) Fatal pulmonary embolism following removal of a central venous catheter. J Pediatr Surg 19:307–309PubMedGoogle Scholar
  35. 35.
    Revel-Vilk S, Massicotte P (2003) Thromboembolic diseases of childhood. Blood Rev 17:1–6Google Scholar
  36. 36.
    Tormene D, Simioni P, Prandoni P, et al (2002) The incidence of venous thromboembolism in thrombophilic children: a prospective cohort study. Blood 100:2403–2405CrossRefPubMedGoogle Scholar
  37. 37.
    Joist JH (2003) What I need to know about thrombophilia. Web site: http://www.slucare.edu/clinical/pathlab/coagulation/thrombophilia.shtml:, pp 1–9
  38. 38.
    Revel-Vilk S, Sharathkumar A, Massicotte P, et al (2004) Natural history of arterial and venous thrombosis in children treated with low molecular weight heparin: a longitudinal study by ultrasound. J Thromb Haemost 2:42–46CrossRefPubMedGoogle Scholar
  39. 39.
    Nuss R, Hays T, Manco-Johnson M (1995) Childhood thrombosis. Pediatrics 96:291–294PubMedGoogle Scholar
  40. 40.
    Berube C, Mitchell L, Silverman E, et al (1998) The relationship of antiphospholipid antibodies to thromboembolic events in pediatric patients with systemic lupus erythematosus: a cross-sectional study. Pediatr Res 44:351–356PubMedGoogle Scholar
  41. 41.
    Tektonidou MG, Malagari K, Vlachoyiannopoulos PG, et al (2003) Asymptomatic avascular necrosis in patients with primary antiphospholipid syndrome in the absence of corticosteroid use: a prospective study by magnetic resonance imaging. Arthritis Rheum 48:732–736CrossRefPubMedGoogle Scholar
  42. 42.
    Ravelli A, Martini A (1997) Antiphospholipid antibody syndrome in pediatric patients. Rheum Dis Clin North Am 23:657–676PubMedGoogle Scholar
  43. 43.
    Kwong T, Leonidas JC, Ilowite NT (1994) Asymptomatic superior vena cava thrombosis and pulmonary embolism in an adolescent with SLE and antiphospholipid antibodies. Clin Exp Rheumatol 12:215–217PubMedGoogle Scholar
  44. 44.
    Stringer MD, Steadman CA, Hedges AR, et al (1989) Deep vein thrombosis after elective knee surgery. An incidence study in 312 patients. J Bone Joint Surg Br 71:492–497PubMedGoogle Scholar
  45. 45.
    Turk EE, Tsokos M (2003) Sudden infant death due to pulmonary embolism. Am J Forensic Med Pathol 24:106CrossRefPubMedGoogle Scholar
  46. 46.
    Crane SD, Beverley DW, Williams MJ (1999) Massive pulmonary embolus in a 14-year-old boy. J Accid Emerg Med 16:289–290PubMedGoogle Scholar
  47. 47.
    van Ommen CH, Ottenkamp J, Lam J, et al (2002) The risk of postthrombotic syndrome in children with congenital heart disease. J Pediatr 141:582–586CrossRefPubMedGoogle Scholar
  48. 48.
    Maeda K, Murakami A, Hishi T, et al (2002) Successful thrombolytic therapy for acute massive pulmonary thrombosis after total cavo-pulmonary shunt. Jpn J Thorac Cardiovasc Surg 50:451–454PubMedGoogle Scholar
  49. 49.
    Aggarwal K, Jain VK, Gupta S, et al (2003) Klippel-Trenaunay syndrome with a life-threatening thromboembolic event. J Dermatol 30:236–240PubMedGoogle Scholar
  50. 50.
    Machin GA, Kent S (1989) Pulmonary thromboembolism from a large hemangioma in a 4-week-old infant. Pediatr Pathol 9(1):73–78PubMedGoogle Scholar
  51. 51.
    Eberhard DA (1994) Two-year-old boy with Proteus syndrome and fatal pulmonary thromboembolism. Pediatr Pathol 14:771–779PubMedGoogle Scholar
  52. 52.
    Uderzo C, Faccini P, Rovelli A, et al (1995) Pulmonary thromboembolism in childhood leukemia: 8-years’ experience in a pediatric hematology center. J Clin Oncol 13:2805–2812PubMedGoogle Scholar
  53. 53.
    Marraro G, Uderzo C, Marchi P, et al (1991) Acute respiratory failure and pulmonary thrombosis in leukemic children. Cancer 67:696–702PubMedGoogle Scholar
  54. 54.
    Mitchell L, Abshire T, Hanna K, et al (1999) A prospective cohort determining the incidence of thrombotic events in children with acute lymphoblastic leukemia treated with L-asparginase: results of the PARKAA study. Blood 94 (Suppl):649aGoogle Scholar
  55. 55.
    Sutor AH, Uhl M (1997) Diagnosis of thromboembolic disease during infancy and childhood. Semin Thromb Hemost 23:237–246PubMedGoogle Scholar
  56. 56.
    Apostol EL, Kher KK (1994) Cavitating pulmonary infarction in nephrotic syndrome. Pediatr Nephrol 8:347–348PubMedGoogle Scholar
  57. 57.
    Huang J, Yang J, Ding J (2000) Pulmonary embolism associated with nephrotic syndrome in children: a preliminary report of 8 cases. Chin Med J (Engl) 113:251–253Google Scholar
  58. 58.
    Oppenheimer EH, Esterly JR (1971) Pulmonary changes in sickle cell disease. Am Rev Respir Dis 103:858–859PubMedGoogle Scholar
  59. 59.
    Sheth S, Ruzal-Shapiro C, Hurlet-Jensen A, et al (1997) Pulmonary embolism developing in patients with sickle cell disease on hypertransfusion and IV deferoxamine chelation therapy. Pediatr Radiol 27:926–928CrossRefPubMedGoogle Scholar
  60. 60.
    Desai MH, Linares HA, Herndon DN (1989) Pulmonary embolism in burned children. Burns 15:376–380PubMedGoogle Scholar
  61. 61.
    Walsh S, Phillips F (2002) Deep vein thrombosis associated with pediatric musculoskeletal sepsis. J Pediatr Orthop 22:329–332CrossRefPubMedGoogle Scholar
  62. 62.
    Gulbahce HE, Manivel JC, Jessurun J (2000) Pulmonary cytolytic thrombi: a previously unrecognized complication of bone marrow transplantation. Am J Surg Pathol 24:1147–1152CrossRefPubMedGoogle Scholar
  63. 63.
    Morales IJ, Anderson PM, Tazelaar HD, et al (2003) Cytolytic thrombi: unusual complication of hematopoietic stem cell transplantation. J Pediatr Hematol Oncol 25:89–92CrossRefPubMedGoogle Scholar
  64. 64.
    Farrell AG, Parikh SR, Darragh RK, et al (1998) Retrieval of “old” foreign bodies from the cardiovascular system in children. Catheter Cardiovasc Diagn 44:212–217CrossRefGoogle Scholar
  65. 65.
    Kjellin IB, Boechat MI, Vinuela F, et al (2000) Pulmonary emboli following therapeutic embolization of cerebral arteriovenous malformations in children. Pediatr Radiol 30:279–283CrossRefPubMedGoogle Scholar
  66. 66.
    Hwang SS, Kim HH, Park SH, et al (2001) N-butyl-2-cyanoacrylate pulmonary embolism after endoscopic injection sclerotherapy for gastric variceal bleeding. J Comput Assist Tomogr 25:16–22CrossRefPubMedGoogle Scholar
  67. 67.
    Carapiet DA, Stevens JE (1996) Pulmonary embolism following embolization of an arteriovenous malformation. Paediatr Anaesth 6:491–494CrossRefPubMedGoogle Scholar
  68. 68.
    Gonzalez A, Altieri PI, Marquez EU, et al (1980) Massive pulmonary embolism associated with a right ventricular myxoma. Am J Med 69:795–798CrossRefPubMedGoogle Scholar
  69. 69.
    Soares FA (2000) Fatal pulmonary tumor embolism caused by chondroblastic osteosarcoma. Arch Pathol Lab Med 124:661PubMedGoogle Scholar
  70. 70.
    Ceelen W, Kerremans I, Lutz-Dettinger N, et al (1997) Wilms’ tumour presenting as a pulmonary embolism. Acta Chir Belg 97:148–150Google Scholar
  71. 71.
    Suzuki T, Ikeda N, Umetsu K, et al (1984) Pulmonary fat embolism as an ante-mortem reaction in traumatic immediate death. Med Sci Law 24:175–178PubMedGoogle Scholar
  72. 72.
    Basso C, Corrado D, Thiene G (1999) Cardiovascular causes of sudden death in young individuals including athletes. Cardiol Rev 7:127–135PubMedGoogle Scholar
  73. 73.
    Thomas DA, de Boisblanc BP, Summer WR (1997) Venous thromboembolism. A contemporary diagnostic and therapeutic approach. Postgrad Med 102:179–181PubMedGoogle Scholar
  74. 74.
    Croyle PH, Place RA, Hilgenberg AD (1979) Massive pulmonary embolism in a high school wrestler. JAMA 241:827–828PubMedGoogle Scholar
  75. 75.
    Worsley DF, Alavi A (1995) Comprehensive analysis of the results of the PIOPED study. Prospective investigation of pulmonary embolism diagnosis study. J Nucl Med 36:2380–2387PubMedGoogle Scholar
  76. 76.
    Chant H, McCollum C (2001) Stroke in young adults: the role of paradoxical embolism. Thromb Haemost 85:22–29PubMedGoogle Scholar
  77. 77.
    Playfor SD, Smyth AR (1999) Paradoxical embolism in a boy with cystic fibrosis and a stroke. Thorax 54:1139–1140PubMedGoogle Scholar
  78. 78.
    Schrecengost JE, LeGallo RD, Boyd JC, et al (2003) Comparison of diagnostic accuracies in outpatients and hospitalized patients of D-dimer testing for the evaluation of suspected pulmonary embolism. Clin Chem 49:1483–1490CrossRefPubMedGoogle Scholar
  79. 79.
    Kearon C (2003) Diagnosis of pulmonary embolism. CMAJ 168:183–194PubMedGoogle Scholar
  80. 80.
    Hirsh J, Lee AY (2002) How we diagnose and treat deep vein thrombosis. Blood 99:3102–3110CrossRefPubMedGoogle Scholar
  81. 81.
    Mitchell L, Chait P, Ginsberg JS, et al (1999) Comparison of venography with ultrasound for detection of venous thrombosis in the upper body in children: results of the PARKAA study. Blood 94(Suppl):588aGoogle Scholar
  82. 82.
    Woodruff WW 3rd, Merten DF, Wagner ML, et al (1986) Chronic pulmonary embolism in children. Radiology 159:511–514PubMedGoogle Scholar
  83. 83.
    The PIOPED Investigators (1990) Value of the ventilation/perfusion scan in acute pulmonary embolism. Results of the prospective investigation of pulmonary embolism diagnosis (PIOPED). JAMA 263:2753–2759PubMedGoogle Scholar
  84. 84.
    Evander E, Holst H, Jarund A, et al (2003) Role of ventilation scintigraphy in diagnosis of acute pulmonary embolism: an evaluation using artificial neural networks. Eur J Nucl Med Mol Imag 30:961–965CrossRefGoogle Scholar
  85. 85.
    Evans DA, Wilmott RW (1994) Pulmonary embolism in children. Pediatr Clin North Am 41:569–584PubMedGoogle Scholar
  86. 86.
    Dicarli MF, Gerbaudo VH, Singh TP, et al (2003) Cardiopulmonary studies in pediatric nuclear medicine (Chapter 57). In: Sandler MP, Coleman RE, Patton JA, et al (eds) Diagnostic nuclear medicine. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  87. 87.
    Marsh JD, Glynn M, Torman HA (1983) Pulmonary angiography. Application in a new spectrum of patients. Am J Med 75:763–770CrossRefPubMedGoogle Scholar
  88. 88.
    Zuckerman DA, Sterling KM, Oser RF (1996) Safety of pulmonary angiography in the 1990s. J Vasc Interv Radiol 7:199–205PubMedGoogle Scholar
  89. 89.
    Kruger S, Haage P, Hoffmann R, et al (2001) Diagnosis of pulmonary arterial hypertension and pulmonary embolism with magnetic resonance angiography. Chest 120:1556–1561CrossRefPubMedGoogle Scholar
  90. 90.
    Hudson ER, Smith TP, McDermott VG, et al (1996) Pulmonary angiography performed with iopamidol: complications in 1,434 patients. Radiology 198:61–65PubMedGoogle Scholar
  91. 91.
    Stein PD, Athanasoulis C, Alavi A, et al (1992) Complications and validity of pulmonary angiography in acute pulmonary embolism. Circulation 85:462–468PubMedGoogle Scholar
  92. 92.
    Hull RD, Raskob GE, Ginsberg JS, et al (1994) A noninvasive strategy for the treatment of patients with suspected pulmonary embolism. Arch Intern Med 154:289–297CrossRefPubMedGoogle Scholar
  93. 93.
    Lombard J, Bhatia R, Sala E (2003) Spiral computed tomographic pulmonary angiography for investigating suspected pulmonary embolism: clinical outcomes. Can Assoc Radiol J 54:147–151PubMedGoogle Scholar
  94. 94.
    Siegel MJ, Luker GD (1995) Pediatric applications of helical (spiral) CT. Radiol Clin North Am 33:997–1022PubMedGoogle Scholar
  95. 95.
    Siegel MJ (2003) Multiplanar and three-dimensional multi-detector row CT of thoracic vessels and airways in the pediatric population. Radiology 229:641–650PubMedGoogle Scholar
  96. 96.
    Halliburton SS, Paschal CB, Rothpletz JD, et al (2001) Estimation and visualization of regional and global pulmonary perfusion with 3-D magnetic resonance angiography. J Magn Reson Imaging 14:734–740CrossRefPubMedGoogle Scholar
  97. 97.
    Goyen M, Laub G, Ladd ME, et al (2001) Dynamic 3-D MR angiography of the pulmonary arteries in under four seconds. J Magn Reson Imaging 13:372–377CrossRefPubMedGoogle Scholar
  98. 98.
    Sonnet S, Buitrago-Tellez CH, Schulte AC, et al (2003) Dose optimization for dynamic time-resolved contrast-enhanced 3-D MR angiography of pulmonary circulation. AJR Am J Roentgenol 181:1499–1503PubMedGoogle Scholar
  99. 99.
    Chalmers EA, Gibson BE (1999) Thrombolytic therapy in the management of paediatric thromboembolic disease. Br J Haematol 104:14–21PubMedGoogle Scholar
  100. 100.
    Andrew M, Michelson AD, Bovill T, et al (1997) The prevention and treatment of thromboembolic disease in children: a need for thrombophilia programs. J Pediatr Hematol Oncol 19:7–22CrossRefPubMedGoogle Scholar
  101. 101.
    Peuster M, Bertram H, Windhagen-Mahnert B, et al (1998) Mechanical recanalization of venous thrombosis and pulmonary embolism with the Clotbuster thrombectomy system in a 12-year-old boy. Z Kardiol 87:283–287CrossRefPubMedGoogle Scholar
  102. 102.
    Reed RA, Teitelbaum GP, Stanley P, et al (1996) The use of inferior vena cava filters in pediatric patients for pulmonary embolus prophylaxis. Cardiovasc Intervent Radiol 19:401–405Google Scholar
  103. 103.
    Khong PL, John PR (1997) Technical aspects of insertion and removal of an inferior vena cava IVC filter for prophylactic treatment of pulmonary embolus. Pediatr Radiol 27:239–241CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Paul S. Babyn
    • 1
  • Harpal K. Gahunia
    • 1
  • Patricia Massicotte
    • 2
  1. 1.Department of Pediatric Diagnostic ImagingThe Hospital for Sick ChildrenTorontoCanada, M5G 1X5
  2. 2.Departments of Pediatric Hematology and CardiologyStollery Children’s Hospital and University of AlbertaEdmontonCanada, T6G 2B7

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