Skip to main content
SpringerLink
Log in

Effect of breath holding at the end of the inspiration and expiration phases on liver stiffness measured by 2D-MR elastography

  • Hepatobiliary
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Purpose

Evaluate the effect of breath holding at the end of the inspiration and expiration phases on the measurement of liver stiffness by 2D-MR elastography (MRE).

Methods

The study included 61 subjects, of which 31 subjects were pathologically confirmed liver fibrosis patients [liver fibrosis group (LFG)] and 30 healthy subjects [healthy group (HG)]. MRE was used to measure the liver stiffness of subjects in inspiration breath-hold (IBH) and expiration breath-hold (EBH) states.

Results

In IBH and EBH states, the liver stiffness measured by MRE was not significantly different in the HG (P = 0.125, > 0.05), while the LFG showed a significant difference (P <0.001). Also, a significant difference was observed between the change values in the mild/moderate fibrosis group (MFG) and advanced fibrosis group (AFG) (P = 0.005, < 0.05).

Conclusions

The liver stiffness values in patients with liver fibrosis were affected by breath-holding states. The higher the stage of liver fibrosis, the greater the change in liver stiffness values, but no significant difference was observed between liver stiffness values in healthy subjects under the two breath-holding conditions. Different breath-holding states are factors influencing liver fibrosis stiffness measured by MRE, which should be given due attention in both clinical and research contexts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets used during the current study are available from the corresponding author on reasonable request.

References

  1. Pellicoro A, Ramachandran P, Iredale JP, Fallowfield JA. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat Rev Immunol. 2014;14(3):181–194. https://doi.org/10.1038/nri3623

    Article  CAS  PubMed  Google Scholar 

  2. Trautwein C, Friedman SL, Schuppan D, Pinzani M. Hepatic fibrosis: Concept to treatment. J Hepatol. 2015;62(1 Suppl):S15–S24. https://doi.org/10.1016/j.jhep.2015.02.039

    Article  CAS  PubMed  Google Scholar 

  3. Marcellin P, Gane E, Buti M, et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet. 2013;381(9865):468–475. https://doi.org/10.1016/S0140-6736(12)61425-1

    Article  CAS  PubMed  Google Scholar 

  4. Lassailly G, Caiazzo R, Buob D, et al. Bariatric Surgery Reduces Features of Nonalcoholic Steatohepatitis in Morbidly Obese Patients. Gastroenterology. 2015;149(2):379‐e16. https://doi.org/10.1053/j.gastro.2015.04.014

    Article  Google Scholar 

  5. Gonzalez HC, Jafri SM, Gordon SC. Role of liver biopsy in the era of direct-acting antivirals. Curr Gastroenterol Rep. 2013;15(2):307. https://doi.org/10.1007/s11894-012-0307-z

    Article  PubMed  Google Scholar 

  6. Gilmore IT, Burroughs A, Murray-Lyon IM, Williams R, Jenkins D, Hopkins A. Indications, methods, and outcomes of percutaneous liver biopsy in England and Wales: an audit by the British Society of Gastroenterology and the Royal College of Physicians of London. Gut. 1995;36(3):437–441. https://doi.org/10.1136/gut.36.3.437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Hennedige TP, Wang G, Leung FP, et al. Magnetic Resonance Elastography and Diffusion Weighted Imaging in the Evaluation of Hepatic Fibrosis in Chronic Hepatitis B. Gut Liver. 2017;11(3):401–408. https://doi.org/10.5009/gnl16079.

    Article  PubMed  Google Scholar 

  8. Besa C, Wagner M, Lo G, et al. Detection of liver fibrosis using qualitative and quantitative MR elastography compared to liver surface nodularity measurement, gadoxetic acid uptake, and serum markers. J Magn Reson Imaging. 2018;47(6):1552–1561. https://doi.org/10.1002/jmri.25911.

    Article  PubMed  Google Scholar 

  9. Choi YR, Lee JM, Yoon JH, Han JK, Choi BI. Comparison of magnetic resonance elastography and gadoxetate disodium-enhanced magnetic resonance imaging for the evaluation of hepatic fibrosis. Invest Radiol. 2013;48(8):607–613. https://doi.org/10.1097/RLI.0b013e318289ff8f

    Article  CAS  PubMed  Google Scholar 

  10. Kim D, Kim WR, Talwalkar JA, Kim HJ, Ehman RL. Advanced fibrosis in nonalcoholic fatty liver disease: noninvasive assessment with MR elastography. Radiology. 2013;268(2):411–419. https://doi.org/10.1148/radiol.13121193

    Article  PubMed  PubMed Central  Google Scholar 

  11. Loomba R, Wolfson T, Ang B, et al. Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study [published correction appears in Hepatology. 2015 Nov;62(5):1646]. Hepatology. 2014;60(6):1920–1928. https://doi.org/10.1002/hep.27362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Batheja M, Vargas H, Silva AM, et al. Magnetic resonance elastography (MRE) in assessing hepatic fibrosis: performance in a cohort of patients with histological data. Abdom Imaging. 2015;40(4):760–765. https://doi.org/10.1007/s00261-014-0321-8

    Article  PubMed  Google Scholar 

  13. Yoshimitsu K, Mitsufuji T, Shinagawa Y, et al. MR elastography of the liver at 3.0 T in diagnosing liver fibrosis grades; preliminary clinical experience. Eur Radiol. 2016;26(3):656–663. https://doi.org/10.1007/s00330-015-3863-4

    Article  PubMed  Google Scholar 

  14. Venkatesh SK, Talwalkar JA. When and how to use magnetic resonance elastography for patients with liver disease in clinical practice. Am J Gastroenterol. 2018;113(7):923–926. https://doi.org/10.1038/s41395-018-0012-0

    Article  PubMed  Google Scholar 

  15. Srinivasa Babu A, Wells ML, Teytelboym OM, et al. Elastography in Chronic Liver Disease: Modalities, Techniques, Limitations, and Future Directions. Radiographics. 2016;36(7):1987–2006. https://doi.org/10.1148/rg.2016160042

    Article  PubMed  PubMed Central  Google Scholar 

  16. Castera L, Foucher J, Bernard PH, et al. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology. 2010; 51:828–835. [PubMed: 20063276]

  17. Zhuo J, Gullapalli RP. AAPM/RSNA physics tutorial for residents: MR artifacts, safety, and quality control. Radiographics. 2006;26(1):275–297. https://doi.org/10.1148/rg.261055134

    Article  PubMed  Google Scholar 

  18. Yin M, Talwalkar JA, Glaser KJ, et al. Dynamic postprandial hepatic stiffness augmentation assessed with MR elastography in patients with chronic liver disease. AJR Am J Roentgenol. 2011;197(1):64–70. https://doi.org/10.2214/AJR.10.5989

    Article  Google Scholar 

  19. Mueller S. Does pressure cause liver cirrhosis? The sinusoidal pressure hypothesis. World J Gastroenterol. 2016;22(48):10482–10501. https://doi.org/10.3748/wjg.v22.i48.10482

    Article  PubMed  PubMed Central  Google Scholar 

  20. Asbach P, Klatt D, Hamhaber U, et al. Assessment of liver viscoelasticity using multifrequency MR elastography. Magn Reson Med. 2008;60(2):373–379. https://doi.org/10.1002/mrm.21636

    Article  PubMed  Google Scholar 

  21. Huwart L, van Beers BE. MR elastography. Gastroenterol Clin Biol. 2008;32(6 Suppl 1):68–72. https://doi.org/10.1016/S0399-8320(08)73995-2

    Article  CAS  PubMed  Google Scholar 

  22. Yin M, Chen J, Glaser KJ, Talwalkar JA, Ehman RL. Abdominal magnetic resonance elastography. Top Magn Reson Imaging. 2009;20(2):79–87. https://doi.org/10.1097/RMR.0b013e3181c4737e

    Article  PubMed  PubMed Central  Google Scholar 

  23. Murphy IG, Graves MJ, Reid S, et al. Comparison of breath-hold, respiratory navigated and free-breathing MR elastography of the liver. Magn Reson Imaging. 2017;37:46–50. https://doi.org/10.1016/j.mri.2016.10.011

    Article  PubMed  Google Scholar 

  24. Altinkaya N, Koc Z, Ulusan S, Demir S, Gurel K. Effects of respiratory manoeuvres on hepatic vein Doppler waveform and flow velocities in a healthy population. Eur J Radiol. 2011;79(1):60–63. https://doi.org/10.1016/j.ejrad.2010.01.011

    Article  PubMed  Google Scholar 

  25. Richardson PD, Withrington PG. Liver blood flow. I. Intrinsic and nervous control of liver blood flow. Gastroenterology. 1981;81(1):159–173.

    Article  CAS  Google Scholar 

  26. Kleiner DE, Brunt EM, Van Natta M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–1321. https://doi.org/10.1002/hep.20701

    Article  PubMed  Google Scholar 

  27. Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology. 1996;24(2):289–293. https://doi.org/10.1002/hep.510240201

    Article  CAS  PubMed  Google Scholar 

  28. Bunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94(9):2467–2474. https://doi.org/10.1111/j.1572-0241.1999.01377.x

    Article  Google Scholar 

  29. Kleiner DE, Brunt EM. Nonalcoholic fatty liver disease: pathologic patterns and biopsy evaluation in clinical research. Semin Liver Dis. 2012;32(1):3–13. https://doi.org/10.1055/s-0032-1306421

    Article  CAS  PubMed  Google Scholar 

  30. Silva AM, Grimm RC, Glaser KJ, et al. Magnetic resonance elastography: evaluation of new inversion algorithm and quantitative analysis method. Abdom Imaging. 2015;40(4):810–817. https://doi.org/10.1007/s00261-015-0372-5

    Article  PubMed  Google Scholar 

  31. Trout AT, Serai S, Mahley AD, et al. Liver Stiffness Measurements with MR Elastography: Agreement and Repeatability across Imaging Systems, Field Strengths, and Pulse Sequences. Radiology. 2016;281(3):793–804. https://doi.org/10.1148/radiol.2016160209

    Article  PubMed  Google Scholar 

  32. Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–191. https://doi.org/10.3758/bf03193146

    Article  PubMed  Google Scholar 

  33. Rabinovici N, Navot N. The relationship between respiration, pressure and flow distribution in the vena cava and portal and hepatic veins. Surg Gynecol Obstet. 1980;151(6):753–763.

    CAS  PubMed  Google Scholar 

  34. Millonig G, Friedrich S, Adolf S, et al. Liver stiffness is directly influenced by central venous pressure. J Hepatol. 2010;52(2):206–210. https://doi.org/10.1016/j.jhep.2009.11.018.

    Article  PubMed  Google Scholar 

  35. Wang K, Manning P, Szeverenyi N, et al. Repeatability and reproducibility of 2D and 3D hepatic MR elastography with rigid and flexible drivers at end-expiration and end-inspiration in healthy volunteers. Abdom Radiol (NY). 2017;42(12):2843–2854. https://doi.org/10.1007/s00261-017-1206-4

    Article  Google Scholar 

  36. Yang YL, Di L, Duan YY, et al. A prospective experimental study of liver fibrosis with ultrasound and its correlation with hepatic reserve function and hemodynamics. BMC Gastroenterol. 2012;12:168. Published 2012 Nov 23. https://doi.org/10.1186/1471-230X-12-168

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a Grant from the National Natural Science Foundation of China (No. 61871276).

Funding

National Natural Science Foundation of China (No. 61871276) National Science and Technology Major Project (2017ZX0203202-003).

Author information

Authors and Affiliations

  1. Department of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, West District, Beijing, 100050, China

    Hao Ren, Dawei Yang, Hui Xu & Zhenghan Yang

  2. Department of General Surgery, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, West District, Beijing, 100050, China

    Kai Pang

  3. Liver Research Center, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, West District, Beijing, 100050, China

    Yiwen Shi & Qiushuang Guan

Authors
  1. Hao Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dawei Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kai Pang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yiwen Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qiushuang Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhenghan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhenghan Yang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures in this study were in accordance with the Ethical Standards of the Institutional Research Committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Written informed consent was obtained from individual or guardian participants.

Consent for publication

Written informed consent for publication was obtained from all participants.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ren, H., Yang, D., Xu, H. et al. Effect of breath holding at the end of the inspiration and expiration phases on liver stiffness measured by 2D-MR elastography. Abdom Radiol 46, 2516–2526 (2021). https://doi.org/10.1007/s00261-020-02893-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-020-02893-w

Keywords

Search

Navigation