Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 8720367, 10 pages
https://doi.org/10.1155/2017/8720367
Research Article

Effects of Liver Fibrosis Progression on Tissue Relaxation Times in Different Mouse Models Assessed by Ultrahigh Field Magnetic Resonance Imaging

1Clinic for Diagnostic and Interventional Radiology, Saarland University Medical Center, Kirrberger Str. 100, Bdg. 50.1, 66421 Homburg, Germany
2Department of Medicine, University of California San Diego, 9500 Gilman Dr, La Jolla, CA 92093, USA
3Department of Internal Medicine II, Saarland University, Saarland University Medical Center, Bdg. 77, Kirrberger Str. 100, 66421 Homburg, Germany
4Institute of Pathology, University Hospital Bonn, Bdg. 62, Sigmund-Freud Str. 25, 53127 Bonn, Germany

Correspondence should be addressed to Peter Fries; ue.sku@seirf.retep

Received 11 October 2016; Accepted 14 December 2016; Published 18 January 2017

Academic Editor: Kim Bridle

Copyright © 2017 Andreas Müller et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Bataller and D. A. Brenner, “Liver fibrosis,” Journal of Clinical Investigation, vol. 115, no. 2, pp. 209–218, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. S. L. Friedman, “Liver fibrosis—from bench to bedside,” Journal of Hepatology, Supplement, vol. 38, no. 1, pp. S38–S53, 2003. View at Google Scholar · View at Scopus
  3. J. P. Iredale, “Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ,” Journal of Clinical Investigation, vol. 117, no. 3, pp. 539–548, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Mallat and S. Lotersztajn, “Cellular mechanisms of tissue fibrosis. 5. novel insights into liver fibrosis,” American Journal of Physiology—Cell Physiology, vol. 305, no. 8, pp. C789–C799, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. S.-J. Lee, K.-H. Kim, and K.-K. Park, “Mechanisms of fibrogenesis in liver cirrhosis: the molecular aspects of epithelial-mesenchymal transition,” World Journal of Hepatology, vol. 6, no. 4, pp. 207–216, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Schuppan and Y. O. Kim, “Evolving therapies for liver fibrosis,” Journal of Clinical Investigation, vol. 123, no. 5, pp. 1887–1901, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. Guo, S. Parthasarathy, P. Goyal, R. J. McCarthy, A. C. Larson, and F. H. Miller, “Magnetic resonance elastography and acoustic radiation force impulse for staging hepatic fibrosis: a meta-analysis,” Abdominal imaging, vol. 40, no. 4, pp. 818–834, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Yin, J. Woollard, X. Wang et al., “Quantitative assessment of hepatic fibrosis in an animal model with magnetic resonance elastography,” Magnetic Resonance in Medicine, vol. 58, no. 2, pp. 346–353, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Polasek, B. C. Fuchs, R. Uppal et al., “Molecular MR imaging of liver fibrosis: a feasibility study using rat and mouse models,” Journal of Hepatology, vol. 57, no. 3, pp. 549–555, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Boursier, S. Bertrais, F. Oberti et al., “Comparison of accuracy of fibrosis degree classifications by liver biopsy and non-invasive tests in chronic hepatitis C,” BMC Gastroenterology, vol. 11, article 132, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Lichtinghagen, D. Pietsch, H. Bantel, M. P. Manns, K. Brand, and M. J. Bahr, “The Enhanced Liver Fibrosis (ELF) score: normal values, influence factors and proposed cut-off values,” Journal of Hepatology, vol. 59, no. 2, pp. 236–242, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. B. C. Fuchs, H. Wang, Y. Yang et al., “Molecular MRI of collagen to diagnose and stage liver fibrosis,” Journal of Hepatology, vol. 59, no. 5, pp. 992–998, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Banerjee, M. Pavlides, E. M. Tunnicliffe et al., “Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease,” Journal of Hepatology, vol. 60, no. 1, pp. 69–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. C. L. Hoad, N. Palaniyappan, P. Kaye et al., “A study of T1 relaxation time as a measure of liver fibrosis and the influence of confounding histological factors,” NMR in Biomedicine, vol. 28, no. 6, pp. 706–714, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Aubé, F. Moal, F. Oberti et al., “Diagnosis and measurement of liver fibrosis by MRI in bile duct ligated rats,” Digestive Diseases and Sciences, vol. 52, no. 10, pp. 2601–2609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. A. M. Chow, D. S. Gao, S. J. Fan et al., “Measurement of liver T1 and T2 relaxation times in an experimental mouse model of liver fibrosis,” Journal of Magnetic Resonance Imaging, vol. 36, no. 1, pp. 152–158, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Jüngst and F. Lammert, “Cholestatic liver disease,” Digestive Diseases, vol. 31, no. 1, pp. 152–154, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Hochrath, M. Krawczyk, R. Goebel et al., “The hepatic phosphatidylcholine transporter ABCB4 as modulator of glucose homeostasis,” FASEB Journal, vol. 26, no. 12, pp. 5081–5091, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. D. W. Marquardt, “An algorithm for least-squares estimation of nonlinear parameters,” Journal of the Society for Industrial and Applied Mathematics, vol. 11, no. 2, pp. 431–441, 1963. View at Google Scholar · View at MathSciNet
  20. D. Hernando, Y. S. Levin, C. B. Sirlin, and S. B. Reeder, “Quantification of liver iron with MRI: state of the art and remaining challenges,” Journal of Magnetic Resonance Imaging, vol. 40, no. 5, pp. 1003–1021, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. I. S. Jamall, V. N. Finelli, and S. S. Q. Hee, “A simple method to determine nanogram levels of 4-hydroxyproline in biological tissues,” Analytical Biochemistry, vol. 112, no. 1, pp. 70–75, 1981. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Hillebrandt, C. Goos, S. Matern, and F. Lammert, “Genome-wide analysis of hepatic fibrosis in inbred mice identifies the susceptibility locus Hfib1 on chromosome 15,” Gastroenterology, vol. 123, no. 6, pp. 2041–2051, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. K. P. Batts and J. Ludwig, “Chronic hepatitis: an update on terminology and reporting,” American Journal of Surgical Pathology, vol. 19, no. 12, pp. 1409–1417, 1995. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Ishak, A. Baptista, L. Bianchi et al., “Histological grading and staging of chronic hepatitis,” Journal of Hepatology, vol. 22, no. 6, pp. 696–699, 1995. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Shimada, T. Nakanishi, A. Toyama et al., “Potential implications for monitoring serum bile acid profiles in circulation with serum proteome for carbon tetrachloride-induced liver injury/regeneration model in mice,” Journal of Proteome Research, vol. 9, no. 9, pp. 4490–4500, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Germani, P. Hytiroglou, A. Fotiadu, A. K. Burroughs, and A. P. Dhillon, “Assessment of fibrosis and cirrhosis in liver biopsies: an update,” Seminars in Liver Disease, vol. 31, no. 1, pp. 82–90, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Bota, H. Herkner, I. Sporea et al., “Meta-analysis: ARFI elastography versus transient elastography for the evaluation of liver fibrosis,” Liver International, vol. 33, no. 8, pp. 1138–1147, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Zhang, Z. Guo, P. Zhang et al., “Simplified quantification method for in vivo SPECT/CT imaging of asialoglycoprotein receptor with 99m Tc-p(VLA-co-VNI) to assess and stage hepatic fibrosis in mice,” Scientific Reports, vol. 6, Article ID 25377, 2016. View at Publisher · View at Google Scholar · View at Scopus
  29. R. A. Hall, R. Liebe, K. Hochrath et al., “Systems genetics of liver fibrosis: identification of fibrogenic and expression quantitative trait loci in the BXD murine reference population,” PLoS ONE, vol. 9, no. 2, Article ID e89279, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. F. W. Smith, J. R. Mallard, A. Reid, and J. M. S. Hutchison, “Nuclear magnetic resonance tomographic imaging in liver disease,” The Lancet, vol. 317, no. 8227, pp. 963–966, 1981. View at Publisher · View at Google Scholar · View at Scopus
  31. F. W. Smith and J. R. Mallard, “NMR imaging in liver disease,” British Medical Bulletin, vol. 40, no. 2, pp. 194–196, 1984. View at Publisher · View at Google Scholar · View at Scopus
  32. D. D. Stark, H. I. Goldberg, A. A. Moss, and N. M. Bass, “Chronic liver disease: evaluation by magnetic resonance,” Radiology, vol. 150, no. 1, pp. 149–151, 1984. View at Publisher · View at Google Scholar · View at Scopus
  33. R. A. F. M. Chamuleau, J. H. N. Creyghton, I. De Nie, M. A. Moerland, O. R. Van der Lende, and J. Smidt, “Is the magnetic resonance imaging proton spin-lattice relaxation time a reliable noninvasive parameter of developing liver fibrosis?” Hepatology, vol. 8, no. 2, pp. 217–221, 1988. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Kreft, F. Dombrowski, W. Block, R. Bachmann, U. Pfeifer, and H. Schild, “Evaluation of different models of experimentally induced liver cirrhosis for MRI research with correlation to histopathologic findings,” Investigative Radiology, vol. 34, no. 5, pp. 360–366, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. H. I. Goldberg, A. A. Moss, D. D. Stark, J. McKerrow, B. Engelstad, and A. Brito, “Hepatic cirrhosis: magnetic resonance imaging,” Radiology, vol. 153, no. 3, pp. 737–739, 1984. View at Publisher · View at Google Scholar · View at Scopus
  36. A. M. Aisen, K. Doi, and S. D. Swanson, “Detection of liver fibrosis with magnetic cross-relaxation,” Magnetic Resonance in Medicine, vol. 31, no. 5, pp. 551–556, 1994. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Fickert, A. Fuchsbichler, M. Wagner et al., “Regurgitation of bile acids from leaky bile ducts causes sclerosing cholangitis in Mdr2 (Abcb4) knockout mice,” Gastroenterology, vol. 127, no. 1, pp. 261–274, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Cavey, M. Ropert, M. De Tayrac et al., “Mouse genetic background impacts both on iron and non-iron metals parameters and on their relationships,” BioMetals, vol. 28, no. 4, pp. 733–743, 2015. View at Publisher · View at Google Scholar · View at Scopus