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Insight into microvascular adaptive alterations in the Glisson system of biliary atresia after Kasai portoenterostomy using X-ray phase-contrast CT

  • Computed Tomography
  • Published:
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Abstract

Objectives

To investigate microvascular alterations in the Glisson system of biliary atresia (BA) patients after Kasai portoenterostomy (KP) using three-dimensional (3D) virtual histopathology based on X-ray phase-contrast CT (PCCT).

Methods

Liver explants from BA patients were imaged using PCCT, and 32 subjects were included and divided into two groups: KP (n = 16) and non-KP (n = 16). Combined with histological analysis and 3D visualization technology, 3D virtual histopathological assessment of the biliary, arterial, and portal venous systems was performed. According to loop volume ratio, 3D spatial density, relative surface area, tortuosity, and other parameters, pathological changes of microvasculature in the Glisson system were investigated.

Results

In the non-KP group, bile ducts mostly manifested as radial multifurcated hyperplasia and twisted into loops. In the KP group, the bile duct hyperplasia was less, and the loop volume ratio of bile ducts decreased by 13.89%. Simultaneously, the arterial and portal venous systems presented adaptive alterations in response to degrees of bile duct hyperplasia. Compared with the non-KP group, the 3D spatial density of arteries in the KP group decreased by 3.53%, and the relative surface area decreased from 0.088 ± 0.035 to 0.039 ± 0.015 (p < .01). Deformed portal branches gradually recovered after KP, with a 2.93% increase in 3D spatial density and a decrease in tortuosity from 1.17 ± 0.06 to 1.14 ± 0.04 (p < .01) compared to the non-KP group.

Conclusion

3D virtual histopathology via PCCT clearly reveals the microvascular structures in the Glisson system of BA patients and provides key insights into the morphological mechanism of microvascular adaptation induced by biliary tract dredging after KP in BA disease.

Key Points

• 3D virtual histopathology via X-ray phase-contrast computed tomography clearly presented the morphological structures and pathological changes of microvasculature in the Glisson system of biliary atresia patients.

• The morphological alterations of microvasculature in the Glisson system followed the competitive occupancy mechanism in the process of biliary atresia.

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Abbreviations

2D:

Two-dimensional

3D:

Three-dimensional

BA:

Biliary atresia

CCD:

Charge-coupled device

CK19:

Cytokeratin 19

FBP:

Filtered back-projection algorithm

HE:

Hematoxylin-eosin

KP:

Kasai portoenterostomy

LT:

Liver transplant

PCCT:

X-ray phase-contrast computed tomography

SMA:

Smooth muscle actin

VOI:

Volumes of interest

References

  1. Hartley JL, Davenport M, Kelly DA (2009) Biliary atresia. Lancet 374:1704–1713

    Article  PubMed  Google Scholar 

  2. Schuppan D, Afdhal NH (2008) Liver cirrhosis. Lancet 371:838–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Sanyal AJ, Bosch J, Blei A, Arroyo V (2008) Portal hypertension and its complications. Gastroenterology 134:1715–1728

    Article  PubMed  Google Scholar 

  4. Aithal GP, Palaniyappan N, China L et al (2021) Guidelines on the management of ascites in cirrhosis. Gut 70:9–29

    Article  PubMed  Google Scholar 

  5. Bezerra JA, Wells RG, Mack CL et al (2018) Biliary atresia: clinical and research challenges for the twenty-first century. Hepatology 68:1163–1173

    Article  PubMed  Google Scholar 

  6. Caruso M, Cuocolo R, Di Dato F et al (2020) Ultrasound, shear-wave elastography, and magnetic resonance imaging in native liver survivor patients with biliary atresia after Kasai portoenterostomy: correlation with medical outcome after treatment. Acta Radiol 61:1300–1308

    Article  PubMed  Google Scholar 

  7. Asai A, Wu JF, Wang KS et al (2022) The outcome of patients with cystic biliary atresia with intact proximal hepatic ducts following hepatic-cyst-jejunostomy. J Pediatr Gastroenterol Nutr 75:131–137

    Article  CAS  PubMed  Google Scholar 

  8. Kato D, Uchida H, Amano H et al (2022) Laparoscopic revision of Kasai portoenterostomy after initial laparoscopic portoenterostomy in patients with biliary atresia: a limited but positive effect on native liver survival. Pediatr Surg Int 38:1821–1827

  9. Okubo R, Nio M, Sasaki H, The Japanese Biliary Atresia Society (2021) Impacts of early Kasai portoenterostomy on short-term and long-term outcomes of biliary atresia. Hepatol Commun 5:234–243

  10. Nio M, Wada M, Sasaki H, Kazama T, Tanaka H, Kudo H (2016) Technical standardization of Kasai portoenterostomy for biliary atresia. J Pediatr Surg 51:2105–2108

    Article  PubMed  Google Scholar 

  11. Yamamoto M, Ariizumi S (2018) Glissonean pedicle approach in liver surgery. Ann Gastroenterol Surg 2:124–128

    Article  PubMed  PubMed Central  Google Scholar 

  12. Oetzmann von Sochaczewski C, Pintelon I, Brouns I et al (2019) Experimentally induced biliary atresia by means of rotavirus-infection is directly linked to severe damage of the microvasculature in the extrahepatic bile duct. Anat Rec 302:818–824

    Article  Google Scholar 

  13. Obayashi J, Tanaka K, Ohyama K et al (2016) Relation between amount of bile ducts in portal canal and outcomes in biliary atresia. Pediatr Surg Int 32:833–838

    Article  PubMed  Google Scholar 

  14. Du J, Shi J, Liu J, Deng C, Shen J, Wang Q (2021) Hemodynamic analysis of hepatic arteries for the early evaluation of hepatic fibrosis in biliary atresia. Comput Methods Prog Biomed 211:106400

    Article  Google Scholar 

  15. Wang Y, Xie X, Cao Q et al (2019) Quantitative contrast-enhanced ultrasound by Sonazoid in the early diagnosis of biliary atresia: an experimental study of rats with bile duct ligation. Ultrasound Med Biol 45:2767–2776

    Article  PubMed  Google Scholar 

  16. Masuya R, Muraji T, Ohtani H et al (2019) Morphometric demonstration of portal vein stenosis and hepatic arterial medial hypertrophy in patients with biliary atresia. Pediatr Surg Int 35:529–537

    Article  PubMed  Google Scholar 

  17. Yang J, Wei N, Su Y, Wei M, Yi B, Feng J (2020) A morphology-based analysis of biliary ductules after Kasai procedure and a review of the literature. J Surg Res 251:180–186

    Article  PubMed  Google Scholar 

  18. Noël PB, Herzen J, Fingerle AA et al (2013) Evaluation of the potential of phase-contrast computed tomography for improved visualization of cancerous human liver tissue. Z Med Phys 23:204–211

    Article  PubMed  Google Scholar 

  19. Kim YH, Kim M-J, Shin HJ et al (2018) MRI-based decision tree model for diagnosis of biliary atresia. Eur Radiol 28:3422–3431

    Article  PubMed  Google Scholar 

  20. Vallonthaiel AG, Baloda V, Singh L et al (2021) Histological analyses of trucut liver biopsies from patients with noncirrhotic portal fibrosis and extra-hepatic portal vein obstruction. Indian J Pathol Microbiol 64:S127–S135

    Article  PubMed  Google Scholar 

  21. Wilkins SW, Gureyev TE, Gao D, Pogany A, Stevenson AW (1996) Phase-contrast imaging using polychromatic hard X-rays. Nature 384:335–338

    Article  CAS  Google Scholar 

  22. Jian J, Zhao X, Qin L et al (2019) Three-dimensional visualization of fibrous tissues in cirrhotic rats via X-ray phase-contrast computed tomography with iodine staining. J Synchrotron Radiat 26:1354–1360

    Article  CAS  PubMed  Google Scholar 

  23. Xin X, Xu H, Jian J et al (2022) A method of three-dimensional branching geometry to differentiate the intrahepatic vascular type in early-stage liver fibrosis using X-ray phase-contrast CT. Eur J Radiol 148:110178

    Article  PubMed  Google Scholar 

  24. Töpperwien M, van der Meer F, Stadelmann C, Salditt T (2020) Correlative x-ray phase-contrast tomography and histology of human brain tissue affected by Alzheimer’s disease. Neuroimage 210:116523

  25. Jiang L, Li C, Li M et al (2021) Simultaneous 3D visualization of the microvascular and neural network in mouse spinal cord using synchrotron radiation micro-computed tomography. Neurosci Bull 37:1469–1480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fingerle AA, Willner M, Herzen J et al (2014) Simulated cystic renal lesions: quantitative X-ray phase-contrast CT—an in vitro phantom study. Radiology 272:739–748

    Article  PubMed  Google Scholar 

  27. Auweter SD, Herzen J, Willner M et al (2014) X-ray phase-contrast imaging of the breast—advances towards clinical implementation. Br J Radiol 87:20130606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sun M, Lv W, Zhao X et al (2020) Vascular branching geometry relating to portal hypertension: a study of liver microvasculature in cirrhotic rats by X-ray phase-contrast computed tomography. Quant Imaging Med Surg 10:116–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Xuan R, Zhao X, Jian J et al (2019) Phase-contrast computed tomography: a correlation study between portal pressure and three dimensional microvasculature of ex vivo liver samples from carbon tetrachloride-induced liver fibrosis in rats. Microvasc Res 125:103884

    Article  CAS  PubMed  Google Scholar 

  30. Lv WJ, Zhao XY, Hu DD, Xin XH, Qin LL, Hu CH (2021) Insight into bile duct reaction to obstruction from a three-dimensional perspective using ex vivo phase-contrast CT. Radiology 299:597–610

    Article  PubMed  Google Scholar 

  31. Xie HL, Deng B, Du GH et al (2020) Methodology development and application of X-ray imaging beamline at SSRF. Nucl Sci Tech 31:102

  32. Yamaguti DCC, da Silva Patrício FR (2011) Morphometrical and immunohistochemical study of intrahepatic bile ducts in biliary atresia. Eur J Gastroenterol Hepatol 23:759–765

    Article  CAS  PubMed  Google Scholar 

  33. Bessho K, Bezerra JA (2011) Biliary atresia: will blocking inflammation tame the disease? Annu Rev Med 62:171–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kim WS, Cheon J-E, Youn BJ et al (2007) Hepatic arterial diameter measured with US: adjunct for US diagnosis of biliary atresia. Radiology 245:549–555

    Article  PubMed  Google Scholar 

  35. Harumatsu T, Muraji T, Masuya R et al (2019) Microvascular proliferation of the portal vein branches in the liver of biliary atresia patients at Kasai operation is associated with a better long-term clinical outcome. Pediatr Surg Int 35:1437–1441

    Article  PubMed  Google Scholar 

  36. Yang L, Mizuochi T, Shivakumar P et al (2018) Regulation of epithelial injury and bile duct obstruction by NLRP3, IL-1R1 in experimental biliary atresia. J Hepatol 69:1136–1144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ortiz-Perez A, Donnelly B, Temple H, Tiao G, Bansal R, Mohanty SK (2020) Innate immunity and pathogenesis of biliary atresia. Front Immunol 11:329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Clotman F (2004) Control of bile duct and hepatic artery development by liver-specific transcription factors. Bull Mem Acad R Med Belg 159:353–357

    CAS  PubMed  Google Scholar 

  39. Fabris L, Cadamuro M, Fiorotto R et al (2006) Effects of angiogenic factor overexpression by human and rodent cholangiocytes in polycystic liver diseases. Hepatology 43:1001–1012

    Article  CAS  PubMed  Google Scholar 

  40. Clotman F, Lannoy VJ, Reber M et al (2002) The onecut transcription factor HNF6 is required for normal development of the biliary tract. Development 129:1819–1828

    Article  CAS  PubMed  Google Scholar 

  41. Patel KR, Harpavat S, Khan Z et al (2020) Biliary atresia patients with successful Kasai portoenterostomy can present with features of obliterative portal venopathy. J Pediatr Gastroenterol Nutr 71:91–98

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Thanks to the BL13HB Beamline and all the staff at Shanghai Synchrotron Radiation Facility.

Funding

This work was supported by the National Natural Science Foundation of China under Grant Nos. 82071922, 82102037, 82001813, and 81671683; and Tianjin Municipal Education Commission under Grant No. 2020KJ208.

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Correspondence to Chun-Hong Hu.

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Qi, BN., Lv, WJ., Jian, JB. et al. Insight into microvascular adaptive alterations in the Glisson system of biliary atresia after Kasai portoenterostomy using X-ray phase-contrast CT. Eur Radiol 33, 4082–4093 (2023). https://doi.org/10.1007/s00330-022-09364-4

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