Iranian Journal of Radiology

Published by: Kowsar
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Could the “Stiff Rim Sign” Be an Indicator of Lysyl Oxidase Activity in Breast Cancer?

Yasemin Kayadibi ORCID 1 , * , Fahrettin Kılıç ORCID 2 , Omer Faruk Karatas 3 , Sennur Ilvan ORCID 4 , Emel Ure Esmerer ORCID 5 , Turgut Kayadibi ORCID 6 and Mehmet Halit Yılmaz 2
Authors Information
1 Department of Radiology, Van Training and Research Hospital, Van, Turkey
2 Department of Radiology, Cerrahpasa Medical Faculty, Istanbul University, Istanbul, Turkey
3 Department of Molecular Biology and Genetics, Erzurum Technical University, Erzurum, Turkey
4 Department of Pathology, Cerrahpasa Medical Faculty, Istanbul University, Istanbul, Turkey
5 Department of Radiology, Hakkari Hospital, Hakkari, Turkey
6 Department of Plastic Surgery, Van Training and Research Hospital, Van, Turkey
Article information
  • Iranian Journal of Radiology: In Press (In Press); e84157
  • Published Online: June 3, 2019
  • Article Type: Research Article
  • Received: September 10, 2018
  • Revised: April 7, 2019
  • Accepted: April 13, 2019
  • DOI: 10.5812/iranjradiol.84157

To Cite: Kayadibi Y, Kılıç F, Karatas O F, Ilvan S, Esmerer E U, et al. Could the “Stiff Rim Sign” Be an Indicator of Lysyl Oxidase Activity in Breast Cancer?, Iran J Radiol. Online ahead of Print ; In Press(In Press):e84157. doi: 10.5812/iranjradiol.84157.

Copyright © 2019, Author(s). This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Objectives
3. Patients and Methods
4. Results
5. Discussion
  • 1. Helleman J, Jansen MP, Ruigrok-Ritstier K, van Staveren IL, Look MP, Meijer-van Gelder ME, et al. Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response. Clin Cancer Res. 2008;14(17):5555-64. doi: 10.1158/1078-0432.CCR-08-0555. [PubMed: 18765548].
  • 2. Tilghman RW, Cowan CR, Mih JD, Koryakina Y, Gioeli D, Slack-Davis JK, et al. Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS One. 2010;5(9). e12905. doi: 10.1371/journal.pone.0012905. [PubMed: 20886123]. [PubMed Central: PMC2944843].
  • 3. Smith-Mungo LI, Kagan HM. Lysyl oxidase: Properties, regulation and multiple functions in biology. Matrix Biol. 1998;16(7):387-98. doi: 10.1016/S0945-053X(98)90012-9. [PubMed: 9524359].
  • 4. Nishioka T, Eustace A, West C. Lysyl oxidase: From basic science to future cancer treatment. Cell Struct Funct. 2012;37(1):75-80. doi: 10.1247/csf.11015. [PubMed: 22453058].
  • 5. Peyrol S, Raccurt M, Gerard F, Gleyzal C, Grimaud JA, Sommer P. Lysyl oxidase gene expression in the stromal reaction to in situ and invasive ductal breast carcinoma. Am J Pathol. 1997;150(2):497-507. [PubMed: 9033266]. [PubMed Central: PMC1858268].
  • 6. Decitre M, Gleyzal C, Raccurt M, Peyrol S, Aubert-Foucher E, Csiszar K, et al. Lysyl oxidase-like protein localizes to sites of de novo fibrinogenesis in fibrosis and in the early stromal reaction of ductal breast carcinomas. Lab Invest. 1998;78(2):143-51. [PubMed: 9484712].
  • 7. Bondareva A, Downey CM, Ayres F, Liu W, Boyd SK, Hallgrimsson B, et al. The lysyl oxidase inhibitor, beta-aminopropionitrile, diminishes the metastatic colonization potential of circulating breast cancer cells. PLoS One. 2009;4(5). e5620. doi: 10.1371/journal.pone.0005620. [PubMed: 19440335]. [PubMed Central: PMC2680032].
  • 8. Barr RG. Breast elastograph. New York: Thieme Publishers; 2015. doi: 10.1055/b-0035-121483.
  • 9. Zhou J, Zhan W, Chang C, Zhang X, Jia Y, Dong Y, et al. Breast lesions: Evaluation with shear wave elastography, with special emphasis on the "stiff rim" sign. Radiology. 2014;272(1):63-72. doi: 10.1148/radiol.14130818. [PubMed: 24661245].
  • 10. Itoh A, Ueno E, Tohno E, Kamma H, Takahashi H, Shiina T, et al. Breast disease: Clinical application of US elastography for diagnosis. Radiology. 2006;239(2):341-50. doi: 10.1148/radiol.2391041676. [PubMed: 16484352].
  • 11. Liu B, Zheng Y, Huang G, Lin M, Shan Q, Lu Y, et al. Breast lesions: Quantitative diagnosis using ultrasound shear wave elastography-A systematic review and meta--analysis. Ultrasound Med Biol. 2016;42(4):835-47. doi: 10.1016/j.ultrasmedbio.2015.10.024. [PubMed: 26778289].
  • 12. Barr RG. Shear wave imaging of the breast: Still on the learning curve. J Ultrasound Med. 2012;31(3):347-50. doi: 10.7863/jum.2012.31.3.347. [PubMed: 22368124].
  • 13. Evans A, Rauchhaus P, Whelehan P, Thomson K, Purdie CA, Jordan LB, et al. Does shear wave ultrasound independently predict axillary lymph node metastasis in women with invasive breast cancer? Breast Cancer Res Treat. 2014;143(1):153-7. doi: 10.1007/s10549-013-2747-z. [PubMed: 24305976]. [PubMed Central: PMC4363519].
  • 14. Wang ZL, Sun L, Li Y, Li N. Relationship between elasticity and collagen fiber content in breast disease: A preliminary report. Ultrasonics. 2015;57:44-9. doi: 10.1016/j.ultras.2014.10.016. [PubMed: 25465961].
  • 15. Barr RG, Zhang Z. Effects of precompression on elasticity imaging of the breast: Development of a clinically useful semiquantitative method of precompression assessment. J Ultrasound Med. 2012;31(6):895-902. doi: 10.7863/jum.2012.31.6.895. [PubMed: 22644686].
  • 16. Skerl K, Vinnicombe S, Giannotti E, Thomson K, Evans A. Influence of region of interest size and ultrasound lesion size on the performance of 2D shear wave elastography (SWE) in solid breast masses. Clin Radiol. 2015;70(12):1421-7. doi: 10.1016/j.crad.2015.08.010. [PubMed: 26455652].
  • 17. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25(4):402-8. doi: 10.1006/meth.2001.1262. [PubMed: 11846609].
  • 18. Tozaki M, Fukuma E. Pattern classification of shear wave elastography images for differential diagnosis between benign and malignant solid breast masses. Acta Radiol. 2011;52(10):1069-75. doi: 10.1258/ar.2011.110276. [PubMed: 22013011].
  • 19. Hayashi M, Yamamoto Y, Ibusuki M, Fujiwara S, Yamamoto S, Tomita S, et al. Evaluation of tumor stiffness by elastography is predictive for pathologic complete response to neoadjuvant chemotherapy in patients with breast cancer. Ann Surg Oncol. 2012;19(9):3042-9. doi: 10.1245/s10434-012-2343-1. [PubMed: 22476757].
  • 20. Hayashi M, Yamamoto Y, Sueta A, Tomiguchi M, Yamamoto-Ibusuki M, Kawasoe T, et al. Associations between elastography findings and clinicopathological factors in breast cancer. Medicine (Baltimore). 2015;94(50). e2290. doi: 10.1097/MD.0000000000002290. [PubMed: 26683963]. [PubMed Central: PMC5058935].
  • 21. Xiao Y, Yu Y, Niu L, Qian M, Deng Z, Qiu W, et al. Quantitative evaluation of peripheral tissue elasticity for ultrasound-detected breast lesions. Clin Radiol. 2016;71(9):896-904. doi: 10.1016/j.crad.2016.06.104. [PubMed: 27349474].
  • 22. Xiang L, Ma F, Yao M, Xu G, Pu H, Liu H, et al. Benign lesion evaluation: Factors causing the "stiff rim" sign in breast tissues using shear-wave elastography. Br J Radiol. 2019;92(1094):20180602. doi: 10.1259/bjr.20180602. [PubMed: 30303694]. [PubMed Central: PMC6404811].
  • 23. Park HS, Shin HJ, Shin KC, Cha JH, Chae EY, Choi WJ, et al. Comparison of peritumoral stromal tissue stiffness obtained by shear wave elastography between benign and malignant breast lesions. Acta Radiol. 2018;59(10):1168-75. doi: 10.1177/0284185117753728. [PubMed: 29359949].
  • 24. Chen LC, Tu SH, Huang CS, Chen CS, Ho CT, Lin HW, et al. Human breast cancer cell metastasis is attenuated by lysyl oxidase inhibitors through down-regulation of focal adhesion kinase and the paxillin-signaling pathway. Breast Cancer Res Treat. 2012;134(3):989-1004. doi: 10.1007/s10549-012-1986-8. [PubMed: 22434522].
  • 25. Patani N, Jiang W, Newbold R, Mokbel K. Prognostic implications of carboxyl-terminus of Hsc70 interacting protein and lysyl-oxidase expression in human breast cancer. J Carcinog. 2010;9:9. doi: 10.4103/1477-3163.72505. [PubMed: 21139993]. [PubMed Central: PMC2997236].
  • 26. Chang JM, Moon WK, Cho N, Kim SJ. Breast mass evaluation: Factors influencing the quality of US elastography. Radiology. 2011;259(1):59-64. doi: 10.1148/radiol.10101414. [PubMed: 21330569].
  • 27. Au FW, Ghai S, Lu FI, Moshonov H, Crystal P. Quantitative shear wave elastography: Correlation with prognostic histologic features and immunohistochemical biomarkers of breast cancer. Acad Radiol. 2015;22(3):269-77. doi: 10.1016/j.acra.2014.10.007. [PubMed: 25666048].
  • 28. Evans A, Whelehan P, Thomson K, McLean D, Brauer K, Purdie C, et al. Invasive breast cancer: Relationship between shear-wave elastographic findings and histologic prognostic factors. Radiology. 2012;263(3):673-7. doi: 10.1148/radiol.12111317. [PubMed: 22523322].
  • 29. Youk JH, Gweon HM, Son EJ, Kim JA, Jeong J. Shear-wave elastography of invasive breast cancer: Correlation between quantitative mean elasticity value and immunohistochemical profile. Breast Cancer Res Treat. 2013;138(1):119-26. doi: 10.1007/s10549-013-2407-3. [PubMed: 23324903].
  • 30. Ganau S, Andreu FJ, Escribano F, Martin A, Tortajada L, Villajos M, et al. Shear-wave elastography and immunohistochemical profiles in invasive breast cancer: Evaluation of maximum and mean elasticity values. Eur J Radiol. 2015;84(4):617-22. doi: 10.1016/j.ejrad.2014.12.020. [PubMed: 25619502].
  • 31. Brkljacic B, Divjak E, Tomasovic-Loncaric C, Tesic V, Ivanac G. Shear-wave sonoelastographic features of invasive lobular breast cancers. Croat Med J. 2016;57(1):42-50. doi: 10.3325/cmj.2016.57.42. [PubMed: 26935613]. [PubMed Central: PMC4800323].
  • 32. Evans A, Whelehan P, Thomson K, Brauer K, Jordan L, Purdie C, et al. Differentiating benign from malignant solid breast masses: value of shear wave elastography according to lesion stiffness combined with greyscale ultrasound according to BI-RADS classification. Br J Cancer. 2012;107(2):224-9. doi: 10.1038/bjc.2012.253. [PubMed: 22691969]. [PubMed Central: PMC3394981].

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