Advertisement

Ultrasound findings in paediatric cholestasis: how to image the patient and what to look for

  • Marco Di SerafinoEmail author
  • Matilde Gioioso
  • Rosa Severino
  • Francesco Esposito
  • Norberto Vezzali
  • Federica Ferro
  • Piernicola Pelliccia
  • Maria Grazia Caprio
  • Raffaele Iorio
  • Gianfranco Vallone
Review Article

Abstract

Paediatric biliary tract and gallbladder diseases include a variety of entities with a wide range of clinical presentations. Cholestasis represents an impaired secretion of bilirubin by hepatocytes, manifesting with high blood levels of conjugated bilirubin and jaundice. Various causes may be involved, which can be recognised analysing blood tests and hepatobiliary imaging, while sometimes liver biopsy or surgery may be necessary. High-resolution real-time ultrasonography is an important tool for differentiation of obstructive and non-obstructive causes of jaundice in infants and children. In this paper, we briefly review the normal anatomy and the ultrasound aspects of main pathologies affecting gallbladder and biliary tree in neonatal and paediatric age.

Keywords

Ultrasonography Cholestasis Choledochal cyst Biliary atresia Cholelithiasis Neonatal sclerosant cholangitis 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and its late amendments. Additional informed consented was obtained from all patients for which identifying information is not included in this article.

Human and animal rights

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. 1.
    Behrman RE (ed) (1992) Nelson textbook of pediatrics, 14th edn. Saunders, Philadelphia, p 478Google Scholar
  2. 2.
    Frank SJ, Kurian J (2016) Three-dimensional sonography of biliary tract disorders. J US Med 35(4):791–804Google Scholar
  3. 3.
    Zhang Y, Wang XL, Li SX, Bai YZ, Ren WD, Xie LM et al (2013) Ultrasonographic dimensions of the common bile duct in Chinese children: results of 343 cases. J Pediatr Surg 48:1892–1896Google Scholar
  4. 4.
    Di Serafino M, Severino R, Gioioso M et al (2019) Pediatric liver ultrasound: a pictorial essay. J Ultrasound.  https://doi.org/10.1007/s40477-018-0352-z Google Scholar
  5. 5.
    Hernanz-Schulman M, Ambrosino MM, Freeman PC, Quinn CB (1995) Common bile duct in children: sonographic dimensions. Radiology 195:193–195Google Scholar
  6. 6.
    Di Serafino M, Vitale V, Severino R, Barbuto L, Vezzali N, Ferro F, Rossi E, Caprio MG, Raia V, Vallone G (2018) Pediatric ultrasonography of the pancreas: normal and abnormal findings. J Ultrasound 25:8.  https://doi.org/10.1007/s40477-018-0348-8 Google Scholar
  7. 7.
    Jeon J, Song SY, Lee KT, Lee KH, Bae MH, Lee JK (2013) Clinical significance and long-term outcome of incidentally found bile duct dilatation. Dig Dis Sci 58:3293–3299Google Scholar
  8. 8.
    Tas A, Koklu S (2012) Unusual cause of common bile duct dilatation in asymptomatic elderly patient: right hepatic artery syndrome. Ann Hepatol 11:150–151Google Scholar
  9. 9.
    Gore RM, Levine MS (2007) Textbook of gastrointestinal radiology, 3rd edn. Elsevier, PhiladelphiaGoogle Scholar
  10. 10.
    Oppong KW, Mitra V, Scott J, Anderson K, Charnley RM, Bonnington S et al (2014) Endoscopic US in patients with normal liver blood tests and unexplained dilatation of common bile duct and or pancreatic duct. Scand J Gastroenterol 49:473–480Google Scholar
  11. 11.
    Kim JE, Lee JK, Lee KT, Park DI, Hyun JG, Paik SW et al (2001) The clinical significance of common bile-duct dilatation in patients without biliary symptoms or causative lesions on ultrasonography. Endoscopy 33:495–500Google Scholar
  12. 12.
    Carroll BA, Oppenheimer DA, Muller HH (1982) High-frequency real-time US of the neonatal biliary system. Radiology 145:437–440Google Scholar
  13. 13.
    Teele RL, Share JC (1991) The liver. In: Teele RL, Share JC (eds) Ultrasonography of infants and children. Saunders, Philadelphia, pp 416–451Google Scholar
  14. 14.
    Soares KC, Arnaoutakis DJ, Kamel I et al (2014) Choledochal cysts: presentation, clinical differentiation, and management. J Am Coll Surg 219:1167–1180Google Scholar
  15. 15.
    Lin SF, Lee HC, Yeung CY, Jiang CB, Chan WT (2014) Common bile duct dilatations in asymptomatic neonates: incidence and prognosis. Gastroenterol Res Pract.  https://doi.org/10.1155/2014/392562 Google Scholar
  16. 16.
    Sato M, Ishida H, Konno K et al (2001) Choledochal cyst due to anomalous pancreatobiliary junction in the adult: sonographic findings. Abdom Imaging 26:395–400Google Scholar
  17. 17.
    Naji O, Hussain A, Baker D, Habib N, El-Hasani S (2009) Obstructive jaundice due to autoimmune cholangiopathy. BMJ Case Rep.  https://doi.org/10.1136/bcr.11.2008.1291 Google Scholar
  18. 18.
    Riederer J (2000) Obstructive jaundice du to sludge in the common bile duct. Dtsch Med Wochenschr 125:11–14Google Scholar
  19. 19.
    Todani Takuji et al (1977) Congenital bile duct cysts. Am J Surg 134(2):263–269Google Scholar
  20. 20.
    Ohashi T, Wakai T, Kubota M et al (2013) Risk of subsequent biliary malignancy in patients undergoing cyst excision for congenital choledochal cysts. J Gastroenterol Hepatol 28:243–247Google Scholar
  21. 21.
    Ahuja AT, Griffith JF et al (2007) Caroli disease. In: Amirsys (ed) Diagnostic imaging: ultrasound, vol 1, pp 36–37Google Scholar
  22. 22.
    Shah OJ, Shera AH, Zargar SA et al (2009) Choledochal cysts in children and adults with contrasting profiles: 11-year experience at a tertiary care center in Kashmir. World J Surg 33:2403–2411Google Scholar
  23. 23.
    Di Serafino M, Mercogliano C, Vallone G (2015) US evaluation of the enteric duplication cyst: the gut signature. J Ultrasound 19(2):131–133Google Scholar
  24. 24.
    Di Serafino M, Severino R, Mercogliano C, Lisanti F, Martino C, Rocca R, Abate R, Salata M, Vallone G, Maroscia D (2016) A complicated ileal duplication cyst in a young adult: the value of the “Gut Signature”. Open J Radiol 6:100–104Google Scholar
  25. 25.
    Segal SR, Sherman NH, Rosenberg HK et al (1994) Ultrasonographic features of gastrointestinal duplications. J US Med 13:863–870Google Scholar
  26. 26.
    Mack CL, Sokol RJ (2005) Unraveling the pathogenesis and etiology of biliary atresia. Pediatr Res 57:87R–94RGoogle Scholar
  27. 27.
    Bezerra JA (2005) Potential etiologies of biliary atresia. Pediatr Transplant 9:646–651Google Scholar
  28. 28.
    Valayer J (1996) Conventional treatment of biliary atresia: long-term results. J Pediatr Surg 31:1546–1551Google Scholar
  29. 29.
    Balistreri WF, Grand R, Hoofnagle JH, Suchy FJ, Ryckman FC, Perlmutter DH et al (1996) Biliary atresia: current concepts and research directions. Summary of a symposium. Hepatology 23:1682–1692Google Scholar
  30. 30.
    Ikeda S, Sera Y, Ohshiro H, Uchino S, Akizuki M, Kondo Y (1998) Gallbladder contraction in biliary atresia: a pitfall of US diagnosis. Pediatr Radiol 28:451–453Google Scholar
  31. 31.
    Nicotra JJ, Kramer SS, Bellah RD, Redd DC (1997) Congenital and acquired biliary disorders in children. Semin Roentgenol 32:215–227Google Scholar
  32. 32.
    Choi SO, Park WH, Lee HJ, Woo SK (1996) ‘Triangular cord’: a sonographic finding applicable in the diagnosis of biliary atresia. J Pediatr Surg 31:363–366Google Scholar
  33. 33.
    Iorio R, Liccardo D, Di Dato F, Puoti MG, Spagnuolo MI, Alberti D, Vallone G (2013) US scanning in infants with biliary atresia: the different implications of biliary tract features and liver echostructure. Ultraschall Med 34(5):463–467Google Scholar
  34. 34.
    Giannattasio A, Cirillo F, Liccardo D, Russo M, Vallone G, Iorio R (2008) Diagnostic role of US for biliary atresia. Radiology 247(3):912Google Scholar
  35. 35.
    Visrutaratna P (2003) Biliary atresia: making the diagnosis by the gallbladder ghost triad. Pediatr Radiol 33:902 (author reply 903) Google Scholar
  36. 36.
    Park WH, Choi SO, Lee HJ, Kim SP, Zeon SK, Lee SL (1997) A new diagnostic approach to biliary atresia with emphasis on the ultrasonographic triangular cord sign: comparison of ultrasonography, hepatobiliary scintigraphy, and liver needle biopsy in the evaluation of infantile cholestasis. J Pediatr Surg 32:1555–1559Google Scholar
  37. 37.
    Lee HJ, Lee SM, Park WH, Choi SO (2003) Objective criteria of triangular cord sign in biliary atresia on US scans. Radiology 229:395–400Google Scholar
  38. 38.
    Choi SO, Park WH, Lee HJ, Woo SK (1996) ‘Triangular cord’: a sonographic finding applicable in the diagnosis of biliary atresia. J Pediatr Surg 31:363–366Google Scholar
  39. 39.
    Di Serafino M, Esposito F, Mercogliano C, Vallone G (2016) The triangular cord sign. Abdom Radiol (NY). 41(9):1867–1868Google Scholar
  40. 40.
    Azuma T, Nakamura T, Nakahira M, Harumoto K, Nakaoka T, Moriuchi T (2003) Pre-operative ultrasonographic diagnosis of biliary atresia–with reference to the presence or absence of the extrahepatic bile duct. Pediatr Surg Int 19:475–477Google Scholar
  41. 41.
    Kim WS, Cheon JE, Youn BJ, Yoo SY, Kim WY, Kim IO et al (2007) Hepatic arterial diameter measured with US: adjunct for US diagnosis of biliary atresia. Radiology 245:549–555Google Scholar
  42. 42.
    Lee MS, Kim MJ, Lee MJ, Yoon CS, Han SJ, Oh JT et al (2009) Biliary atresia: color doppler US findings in neonates and infants. Radiology 252:282–289Google Scholar
  43. 43.
    El-Guindi MA, Sira MM, Konsowa HA, El-Abd OL, Salem TA (2013) Value of hepatic subcapsular flow by color Doppler ultrasonography in the diagnosis of biliary atresia. J Gastroenterol Hepatol 28:867–872Google Scholar
  44. 44.
    Burton EM, Babcock DS, Heubi JE, Gelfand MJ (1990) Neonatal jaundice: clinical and ultrasonographic findings. South Med J 83:294–302Google Scholar
  45. 45.
    Kirks DR, Coleman RE, Filston HC, Rosenberg ER, Merten DF (1984) An imaging approach to persistent neonatal jaundice. AJR Am J Roentgenol 142:461–465Google Scholar
  46. 46.
    Takamizawa S, Zaima A, Muraji T, Kanegawa K, Akasaka Y, Satoh S et al (2007) Can biliary atresia be diagnosed by ultrasonography alone? J Pediatr Surg 42:2093–2096Google Scholar
  47. 47.
    Park WH, Choi SO, Lee HJ (1999) The ultrasonographic ‘triangular cord’ coupled with gallbladder images in the diagnostic prediction of biliary atresia from infantile intrahepatic cholestasis. J Pediatr Surg 34:1706–1710Google Scholar
  48. 48.
    Lee SY, Kim GC, Choe BH, Ryeom HK, Jang YJ, Kim HJ et al (2011) Efficacy of US-guided percutaneous cholecystocholangiography for the early exclusion and type determination of biliary atresia. Radiology 261:916–922Google Scholar
  49. 49.
    Kanegawa K, Akasaka Y, Kitamura E, Nishiyama S, Muraji T, Nishijima E et al (2003) Sonographic diagnosis of biliary atresia in pediatric patients using the “triangular cord” sign versus gallbladder length and contraction. AJR Am J Roentgenol 181:1387–1390Google Scholar
  50. 50.
    Mittal V, Saxena AK, Sodhi KS, Thapa BR, Rao KL, Das A et al (2011) Role of abdominal sonography in the preoperative diagnosis of extrahepatic biliary atresia in infants younger than 90 days. AJR Am J Roentgenol 196:W438–W445Google Scholar
  51. 51.
    Han SJ, Kim MJ, Han A, Chung KS, Yoon CS, Kim D et al (2002) Magnetic resonance cholangiography for the diagnosis of biliary atresia. J Pediatr Surg 37:599–604Google Scholar
  52. 52.
    Liu B, Cai J, Xu Y, Peng X, Zheng H, Huang K et al (2014) Three-dimensional magnetic resonance cholangiopancreatography for the diagnosis of biliary atresia in infants and neonates. PLoS One 9:e88268Google Scholar
  53. 53.
    Lee SM, Cheon JE, Choi YH, Kim WS, Cho HH, Kim IO, You SK (2015) Ultrasonographic diagnosis of biliary atresia based on a decision-making tree model Korean. J Radiol 16(6):1364–1372Google Scholar
  54. 54.
    Ikeda S, Sera Y, Ohshiro H, Uchino S, Akizuki M, Kondo Y (1998) Gallbladder contraction in biliary atresia: a pitfall of US diagnosis. Pediatr Radiol 28(6):451–453Google Scholar
  55. 55.
    Han SJ, Kim MJ, Han A, Chung KS, Yoon CS, Kim D, Hwang EH (2002) J magnetic resonance cholangiography for the diagnosis of biliary atresia. Pediatr Surg. 37(4):599–604Google Scholar
  56. 56.
    Tang ST, Li SW, Ying Y, Mao YZ, Yong W, Tong QS (2009) The evaluation of laparoscopy-assisted cholangiography in the diagnosis of prolonged jaundice in infants. J Laparoendosc Adv Surg Tech A 19(6):827–830Google Scholar
  57. 57.
    Bălănescu RN, Bălănescu L, Drăgan G, Moga A, Caragaåã R (2015) Biliary lithiasis with choledocolithiasis in children. Chirurgia (Bucur). 110(6):559–561Google Scholar
  58. 58.
    Jeanty C, Derderian SC, Courtier J, Hirose S (2015) Clinical management of infantile cholelithiasis. J Pediatr Surg 50(8):1289–1292Google Scholar
  59. 59.
    Wesdorp I, Bosman D, de Graaff A et al (2000) Clinical presentations and predisposing factors of cholelithiasis and sludge in children. JPGN 31:411–417Google Scholar
  60. 60.
    Della Corte C, Falchetti D, Nebbia G et al (2008) Management of cholelithiasis in Italian children: a national multicenter study. World J Gastroenterol 14:1383–1388Google Scholar
  61. 61.
    Matos C, Avni EF, Van Gansbeke D, Pardou A, Struyven J (1987) Total parenteral nutrition (TPN) and gallbladder diseases in neonates. Sonographic assessment. J Ultrasound Med 6(5):243–248Google Scholar
  62. 62.
    Poffenberger C, Gausche-Hill M, Ngai S et al (2012) Cholelithiasis and its complications in children and adolescents. Pediatr Emerg Care 28:68–79Google Scholar
  63. 63.
    Svensson J, Makin E (2012) Gallstone disease in children. Semin Pediatr Surg 21:255–265Google Scholar
  64. 64.
    Rothstein D, Harmon CM (2016) Gallbladder disease in children. Sem Ped Surg 25:225–231Google Scholar
  65. 65.
    Amedee-Manesme O, Bernard O, Brunelle F, Hadchouel M, Polonovski C, Baudon JJ, Beguet P et al (1987) Sclerosing cholangitis with neonatal onset. J Pediatr 111:225–229Google Scholar
  66. 66.
    Baker AJ, Portmann B, Westaby D, Wilkinson M, Karani J, Mowat AP (1993) Neonatal sclerosing cholangitis in two siblings: a category of progressive intrahepatic cholestasis. J Pediatr Gastroenterol Nutr 17:317–322Google Scholar

Copyright information

© Società Italiana di Ultrasonologia in Medicina e Biologia (SIUMB) 2019

Authors and Affiliations

  • Marco Di Serafino
    • 1
    Email author
  • Matilde Gioioso
    • 2
  • Rosa Severino
    • 2
  • Francesco Esposito
    • 3
  • Norberto Vezzali
    • 4
  • Federica Ferro
    • 4
  • Piernicola Pelliccia
    • 5
  • Maria Grazia Caprio
    • 6
  • Raffaele Iorio
    • 7
  • Gianfranco Vallone
    • 8
  1. 1.Department of Radiology“Antonio Cardarelli” HospitalNaplesItaly
  2. 2.Department of Radiology“San Carlo Regional Hospital”PotenzaItaly
  3. 3.Department of Radiology“Santobono-Pausilipon” Children HospitalNaplesItaly
  4. 4.Department of Radiology“Regional Hospital of Bolzano”BolzanoItaly
  5. 5.Department of PaediatricsUniversity of Chieti-PescaraChietiItaly
  6. 6.Institute of Biostructure and Bioimaging IBBItalian National Research Council CNRRomeItaly
  7. 7.Department of Paediatrics“Federico II” University HospitalNaplesItaly
  8. 8.Department of Radiology“Federico II” University HospitalNaplesItaly

Personalised recommendations