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Liver parenchymal changes detected by MR elastography and diffusion-weighted imaging after stereotactic body radiotherapy for hepatocellular carcinoma

  • Hepatobiliary
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Abstract

Background

Stereotactic body radiotherapy (SBRT) is a local treatment option for hepatocellular carcinoma (HCC). SBRT-induced focal reactions on the liver parenchyma have not been thoroughly evaluated using quantitative magnetic resonance imaging (MRI).

Purpose

To quantitatively evaluate liver parenchymal changes caused by SBRT for HCC using magnetic resonance elastography (MRE) and diffusion-weighted imaging (DWI).

Method

We retrospectively evaluated 22 adult patients who received SBRT for HCC and 27 who received locoregional therapy other than SBRT (controls). Liver stiffness by MRE and apparent diffusion coefficient (ADC) values by DWI of the liver parenchyma were measured before and after SBRT. Regions of interest (ROIs) were drawn on the two areas of radiation dose distribution levels, > 30 Gy and ≤ 30 Gy; a ROI was drawn in the control group. The two indices were compared before and after SBRT using a Wilcoxon matched-pairs signed-rank test.

Results

Liver stiffness and ADC values were significantly increased after SBRT in the dose areas of > 30 Gy compared with those before SBRT (4.05 vs 4.85 kPa; p < 0.05 in liver stiffness, and 1.10 vs 1.40 ×10−3 s/mm2; p < 0.05 in ADC values). In the dose area of ≦ 30 Gy, liver stiffness showed a significant increase in one reader (p = 0.033) but not in another reader (p = 0.085); ADC value showed no significant difference before and after SBRT as per both readers (p > 0.05). The control group demonstrated no significant differences before and after treatment (p > 0.05).

Conclusion

MRE and DWI can be used to detect SBRT-induced liver parenchymal changes.

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Data availability

The data that support the findings of this study are available on request from the corresponding author.

References

  1. D.I. Tsilimigras, H. Aziz, T.M. Pawlik (2022) Critical Analysis of the Updated Barcelona Clinic Liver Cancer (BCLC) Group Guidelines. Ann Surg Oncol:29 7231-7234.https://doi.org/10.1245/s10434-022-12242-4

    Article  PubMed  Google Scholar 

  2. A. Takeda, N. Sanuki, Y. Tsurugai, S. Iwabuchi, K. Matsunaga, H. Ebinuma, K. Imajo, Y. Aoki, H. Saito, E. Kunieda (2016) Phase 2 study of stereotactic body radiotherapy and optional transarterial chemoembolization for solitary hepatocellular carcinoma not amenable to resection and radiofrequency ablation. Cancer:122 2041-9.https://doi.org/10.1002/cncr.30008

    Article  PubMed  Google Scholar 

  3. F. Wang, K. Numata, A. Takeda, K. Ogushi, H. Fukuda, K. Hara, M. Chuma, T. Eriguchi, Y. Tsurugai, S. Maeda (2021) Safety and efficacy study: Short-term application of radiofrequency ablation and stereotactic body radiotherapy for Barcelona Clinical Liver Cancer stage 0-B1 hepatocellular carcinoma. PLoS One:16 e0245076.https://doi.org/10.1371/journal.pone.0245076

  4. T.S. Lawrence, J.M. Robertson, M.S. Anscher, R.L. Jirtle, W.D. Ensminger, L.F. Fajardo (1995) Hepatic toxicity resulting from cancer treatment. Int J Radiat Oncol Biol Phys:31 1237-48.https://doi.org/10.1016/0360-3016(94)00418-K

    Article  CAS  PubMed  Google Scholar 

  5. C. Guha, B.D. Kavanagh (2011) Hepatic radiation toxicity: avoidance and amelioration. Semin Radiat Oncol:21 256-63.https://doi.org/10.1016/j.semradonc.2011.05.003

    Article  PubMed  PubMed Central  Google Scholar 

  6. A. Mendez Romero, W. Wunderink, S.M. Hussain, J.A. De Pooter, B.J. Heijmen, P.C. Nowak, J.J. Nuyttens, R.P. Brandwijk, C. Verhoef, J.N. Ijzermans, P.C. Levendag (2006) Stereotactic body radiation therapy for primary and metastatic liver tumors: A single institution phase i-ii study. Acta Oncol:45 831-7.https://doi.org/10.1080/02841860600897934

    Article  PubMed  Google Scholar 

  7. A. Moore, M. Cohen-Naftaly, A. Tobar, Y. Kundel, O. Benjaminov, M. Braun, A. Issachar, E. Mor, M. Sarfaty, D. Bragilovski, R.B. Hur, N. Gordon, S.M. Stemmer, A.M. Allen (2017) Stereotactic body radiation therapy (SBRT) for definitive treatment and as a bridge to liver transplantation in early stage inoperable Hepatocellular carcinoma. Radiat Oncol:12 163.https://doi.org/10.1186/s13014-017-0899-4

  8. K.K. Herfarth, H. Hof, M.L. Bahner, F. Lohr, A. Hoss, G. van Kaick, M. Wannenmacher, J. Debus (2003) Assessment of focal liver reaction by multiphasic CT after stereotactic single-dose radiotherapy of liver tumors. Int J Radiat Oncol Biol Phys:57 444-51.https://doi.org/10.1016/s0360-3016(03)00586-8

    Article  PubMed  Google Scholar 

  9. N. Sanuki, A. Takeda, Y. Oku, T. Eriguchi, S. Nishimura, Y. Aoki, T. Mizuno, S. Iwabuchi, E. Kunieda (2014) Threshold doses for focal liver reaction after stereotactic ablative body radiation therapy for small hepatocellular carcinoma depend on liver function: evaluation on magnetic resonance imaging with Gd-EOB-DTPA. Int J Radiat Oncol Biol Phys:88 306-11.https://doi.org/10.1016/j.ijrobp.2013.10.045

    Article  PubMed  Google Scholar 

  10. S.H. Jung, J.I. Yu, H.C. Park, D.H. Lim, Y. Han (2016) A feasibility study evaluating the relationship between dose and focal liver reaction in stereotactic ablative radiotherapy for liver cancer based on intensity change of Gd-EOB-DTPA-enhanced magnetic resonance images. Radiat Oncol J:34 64-75.https://doi.org/10.3857/roj.2016.34.1.64

    Article  PubMed  PubMed Central  Google Scholar 

  11. M.J. Park, S.Y. Kim, S.M. Yoon, J.H. Kim, S.H. Park, S.S. Lee, Y. Lee, M.G. Lee (2014) Stereotactic body radiotherapy-induced arterial hypervascularity of non-tumorous hepatic parenchyma in patients with hepatocellular carcinoma: potential pitfalls in tumor response evaluation on multiphase computed tomography. PLoS One:9 e90327.https://doi.org/10.1371/journal.pone.0090327

  12. S. Takamatsu, K. Kozaka, S. Kobayashi, N. Yoneda, K. Yoshida, D. Inoue, A. Kitao, T. Ogi, T. Minami, W. Kouda, T. Kumano, N. Fuwa, O. Matsui, T. Gabata (2018) Pathology and images of radiation-induced hepatitis: a review article. Jpn J Radiol:36 241-256.https://doi.org/10.1007/s11604-018-0728-1

    Article  PubMed  Google Scholar 

  13. M.M. Haddad, K.W. Merrell, C.L. Hallemeier, G.B. Johnson, T. Mounajjed, K.R. Olivier, J.L. Fidler, S.K. Venkatesh (2016) Stereotactic body radiation therapy of liver tumors: post-treatment appearances and evaluation of treatment response: a pictorial review. Abdom Radiol (NY):41 2061-77.https://doi.org/10.1007/s00261-016-0768-x

    Article  PubMed  Google Scholar 

  14. P.J. Navin, M.C. Olson, M. Mendiratta-Lala, C.L. Hallemeier, M.S. Torbenson, S.K. Venkatesh (2022) Imaging Features in the Liver after Stereotactic Body Radiation Therapy. Radiographics 220084.https://doi.org/10.1148/rg.220084

  15. M. Yin, K.J. Glaser, A. Manduca, T. Mounajjed, H. Malhi, D.A. Simonetto, R. Wang, L. Yang, S.A. Mao, J.M. Glorioso, F.M. Elgilani, C.J. Ward, P.C. Harris, S.L. Nyberg, V.H. Shah, R.L. Ehman (2017) Distinguishing between Hepatic Inflammation and Fibrosis with MR Elastography. Radiology:284 694-705.https://doi.org/10.1148/radiol.2017160622

    Article  PubMed  Google Scholar 

  16. J.J. Yoo, Y.S. Seo, Y.S. Kim, S.W. Jeong, J.Y. Jang, S.J. Suh, H.J. Yim, K.T. Suk, D.J. Kim, K.H. Han, S.U. Kim, B. Lee, S.G. Kim (2019) The Influence of Histologic Inflammation on the Improvement of Liver Stiffness Values Over 1 and 3 Years. J Clin Med:8.https://doi.org/10.3390/jcm8122065

  17. B. Taouli, M. Chouli, A.J. Martin, A. Qayyum, F.V. Coakley, V. Vilgrain (2008) Chronic hepatitis: role of diffusion-weighted imaging and diffusion tensor imaging for the diagnosis of liver fibrosis and inflammation. J Magn Reson Imaging:28 89-95.https://doi.org/10.1002/jmri.21227

    Article  PubMed  Google Scholar 

  18. M. Franca, L. Marti-Bonmati, A. Alberich-Bayarri, P. Oliveira, S. Guimaraes, J. Oliveira, J. Amorim, J.S. Gonzalez, J.R. Vizcaino, H.P. Miranda (2017) Evaluation of fibrosis and inflammation in diffuse liver diseases using intravoxel incoherent motion diffusion-weighted MR imaging. Abdom Radiol (NY):42 468-477.https://doi.org/10.1007/s00261-016-0899-0

    Article  PubMed  Google Scholar 

  19. S. Ichikawa, U. Motosugi, M. Oguri, H. Onishi (2017) Magnetic resonance elastography for prediction of radiation-induced liver disease after stereotactic body radiation therapy. Hepatology:66 664-665.https://doi.org/10.1002/hep.29128

    Article  PubMed  Google Scholar 

  20. C.C. Olsen, J. Welsh, B.D. Kavanagh, W. Franklin, M. McCarter, H.R. Cardenes, L.E. Gaspar, T.E. Schefter (2009) Microscopic and macroscopic tumor and parenchymal effects of liver stereotactic body radiotherapy. Int J Radiat Oncol Biol Phys:73 1414-24.https://doi.org/10.1016/j.ijrobp.2008.07.032

    Article  CAS  PubMed  Google Scholar 

  21. F.F. Guglielmo, S.K. Venkatesh, D.G. Mitchell (2019) Liver MR Elastography Technique and Image Interpretation: Pearls and Pitfalls. Radiographics:39 1983-2002.https://doi.org/10.1148/rg.2019190034

    Article  PubMed  Google Scholar 

  22. J.R. Landis, G.G. Koch (1977) The measurement of observer agreement for categorical data. Biometrics:33 159-74

    Article  CAS  PubMed  Google Scholar 

  23. C.W. Song, E. Glatstein, L.B. Marks, B. Emami, J. Grimm, P.W. Sperduto, M.S. Kim, S. Hui, K.E. Dusenbery, L.C. Cho (2021) Biological Principles of Stereotactic Body Radiation Therapy (SBRT) and Stereotactic Radiation Surgery (SRS): Indirect Cell Death. Int J Radiat Oncol Biol Phys:110 21-34.https://doi.org/10.1016/j.ijrobp.2019.02.047

    Article  PubMed  Google Scholar 

  24. T. Kimura, S. Takahashi, I. Takahashi, I. Nishibuchi, Y. Doi, M. Kenjo, Y. Murakami, Y. Honda, H. Aikata, K. Chayama, Y. Nagata (2015) The Time Course of Dynamic Computed Tomographic Appearance of Radiation Injury to the Cirrhotic Liver Following Stereotactic Body Radiation Therapy for Hepatocellular Carcinoma. PLoS One:10 e0125231.https://doi.org/10.1371/journal.pone.0125231

  25. C.L. Eccles, E.A. Haider, M.A. Haider, S. Fung, G. Lockwood, L.A. Dawson (2009) Change in diffusion weighted MRI during liver cancer radiotherapy: preliminary observations. Acta Oncol:48 1034-43.https://doi.org/10.1080/02841860903099972

    Article  PubMed  Google Scholar 

  26. M. Okada, K. Numata, H. Nihonmatsu, K. Tomita, A. Takeda, K. Tago, T. Hyodo, T. Eriguchi, M. Nakano (2022) Pathological Appearance of Focal Liver Reactions after Radiotherapy for Hepatocellular Carcinoma. Diagnostics (Basel):12.https://doi.org/10.3390/diagnostics12051072

  27. T.R. Chapman, A.R. Kumarapeli, M.J. Nyflot, S.R. Bowen, R.S. Yeung, H.J. Vesselle, M.M. Yeh, S. Apisarnthanarax (2015) Functional imaging of radiation liver injury in a liver metastasis patient: imaging and pathologic correlation. J Gastrointest Oncol:6 E44-7.https://doi.org/10.3978/j.issn.2078-6891.2015.002

    Article  PubMed  PubMed Central  Google Scholar 

  28. M. Sorensen, M.M. Fode, J.B. Petersen, M.I. Holt, M. Hoyer (2021) Effect of stereotactic body radiotherapy on regional metabolic liver function investigated in patients by dynamic [(18)F]FDGal PET/CT. Radiat Oncol:16 192.https://doi.org/10.1186/s13014-021-01909-z

  29. M. Kong, S.E. Hong (2015) Optimal follow-up duration for evaluating objective response to radiotherapy in patients with hepatocellular carcinoma: a retrospective study. Chin J Cancer:34 79-85.https://doi.org/10.5732/cjc.014.10136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Editage (www.editage.com) for English language editing.

Funding

There is no financial support related to this study.

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Authors and Affiliations

  1. Department of Radiology, University of Yamanashi, 1110 Shimokato, Chuo, Yamanashi, 409-3898, Japan

    Yoshie Omiya, Hiroyuki Morisaka, Masaki Matsuda, Masahide Saito & Hiroshi Onishi

  2. Department of Radiology, Kofu Municipal Hospital, Masutsubocho, Kofu, 400-0832, Japan

    Takaaki Hashimoto

  3. Department of Radiology, Kofu-Kyoritsu Hospital, Takara, Kofu, Yamanashi, 400-0034, Japan

    Utaroh Motosugi

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  1. Yoshie Omiya
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Correspondence to Yoshie Omiya.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Since this study was an observational study based on medical records, information on the implementation of the study including the purpose was posted on the website of the Ethics Committee of University of Yamanashi to guarantee the opportunity for the research subjects to refuse.

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Omiya, Y., Morisaka, H., Matsuda, M. et al. Liver parenchymal changes detected by MR elastography and diffusion-weighted imaging after stereotactic body radiotherapy for hepatocellular carcinoma. Abdom Radiol 48, 3353–3361 (2023). https://doi.org/10.1007/s00261-023-03995-x

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